COOPERATIVE NORTH CENTRAL REGIONAL RESEARCH PROJECTPROJECT NUMBER: NC1142

TITLE: Regulation of Photosynthetic ProcessesDURATION: 1 October 2002 - 30 September 2007

STATEMENT OF THE ISSUES AND JUSTIFICATION

Photosynthesis is the primary determinant of crop productivity. It is the single process on earth that converts sunlight into biomass, sequesters atmospheric CO2 into carbohydrates, and liberates O2. Photosynthesis and the resulting yields of food and fiber products are dramatically limited by environmental constraints in agricultural contexts as reflected by the fact that average yields are typically much less than the maximal yields possible when efficiency and sustainability concerns are relaxed.

Whereas agricultural productivity continues to increase slowly, the rate of increase has declined steadily since the 1960’s, and it may soon plateau (Mann, 1998). Thus, there is increasing concern that future increases, essential to enhance the competitiveness of U.S. agriculture and to fulfill global demands for food and fiber, will be dependent on the development of new approaches to increase the capacity of crop plants to produce the nutrients that support the growth of harvested plant parts. New approaches will also be required to enhance efficiency and to improve agricultural sustainability. To achieve these goals, it will be essential to gain fundamental knowledge of the underlying metabolic components that control assimilate production and utilization, and hence plant growth and development. This knowledge must include an understanding of the regulation of important photosynthetic enzymes and how environmental and developmental signals affecting photosynthetic processes are perceived at the molecular and gene levels. Such knowledge will provide new opportunities for crop improvement using the techniques of both molecular genetics and classical breeding.

The proposed multistate research project brings together some of the most outstanding, productive photosynthesis investigators in the country in an integrated effort to broaden our understanding of critically important areas of photosynthesis research. We propose a synergistic, cooperative research program that concentrates on four areas of photosynthetic regulation:

1. Photochemistry and the biogenesis of the photosynthetic apparatus. The purpose of this research is to understand the structure and function of the light harvesting and electron transfer components of the thylakoid membrane, with emphasis on Photosystem I and the mechanisms that control the stoichiometry between Photosystems I and II. Anterograde and retrograde pathways involved in coordinating the expression of nuclear and chloroplast genes for photosynthetic proteins will be studied, and novel photosynthetic proteins will be identified. The collaborating units include IA-AES, NE-AES and OR-AES (3 institutions, 4 research labs).

2. Photosynthetic capture and photorespiratory release of CO2. The goal of this research is to determine and modify the biochemical and regulatory factors that impact photosynthetic capture and photorespiratory release of CO2. Particular emphasis will be placed on understanding protein-protein interactions and post-translational modifications of key photosynthetic enzymes

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involved in primary and secondary CO2 assimilation, as well as the mechanisms that control carbon flux through primary and secondary metabolic pathways. The collaborating units include IL-ARS, KY-AES, MO-AES, NE-AES, and NV-AES (5 institutions, 6 research labs).

3. Mechanisms regulating photosynthate partitioning. The objective of this research is to gain insight into the mechanisms that regulate photosynthate partitioning into pathways of biosynthesis and use of sucrose, starch, and sugar alcohols. These studies will examine interactions between compartments of the cell, between plant parts, and the partitioning of carbohydrates between transport, storage, and stress-protective functions. The collaborating units include FL-AES, IA-AES, IL-AES, MI-AES, MN-AES, NC-AES, NE-AES, PA-AES, SC-AES, WA-AES, WI-AES (11 institutions, 13 research labs).

4. Developmental and environmental limitations to photosynthesis. The aim of this research is to analyze the limitations and environmental factors that influence photosynthetic productivity at the whole plant and canopy levels. Particular emphasis will be placed on abiotic stresses (temperature, water, and salinity), nitrogen use, and global atmospheric change. This work will integrate understanding developed here and under objectives 1 through 3 to optimize photosynthetic production and yield under current and future environmental conditions. The collaborating units include Guam-AES, IA-AES, IL-AES, KS-AES, MI-AES, MS-ARS, NE-AES, NV-AES, OR-AES, WA-AES (10 institutions, 14 research labs).

RELATED, CURRENT AND PREVIOUS WORK

Objective 1: Photochemistry and the Biogenesis of the Photosynthetic Apparatus

Radiant energy is harvested by pigment arrays on thylakoid membranes and stabilized as NADPH and ATP by the coupling of electron transport with ATP biosynthesis. These processes are carried out by membrane complexes that include photosystem I (PSI), photosystem II (PSII), the cytochrome b6/f complex and the ATP synthase. Much progress has been made toward understanding the architecture and function of these complexes, and NC-142 contributions to this effort have been notable, particularly in the area of PSI (Chitnis, 2001). Another important area of investigation concerns the regulatory networks that modulate electron transport processes in response to varying supplies of the substrate (light), or in response to changes in the metabolic demands for the products (ATP and NADPH). As a prominent example, plants and other photosynthetic organisms, including cyanobacteria, achieve proper electron flow rates by regulating the ratio of the two photosystems. The Chitnis (IA-AES) and Rodermel (IA-AES) labs have generated mutants of Arabidopsis and cyanobacteria with altered PSI/PSII stoichiometries (Chen et al., 2000), and characterization of these mutants should lend insight into the responsible regulatory mechanisms.

The biogenesis of the photosynthetic apparatus requires the concerted action of nuclear and chloroplast genes (Rodermel, 2001). Only about 100 of the estimated 2,500 chloroplast proteins are coded for by genes in the chloroplast genome; the rest are coded for by nuclear genes (Martin and Herrmann, 1998). Although many of the best-characterized biochemical pathways in plants take place in chloroplasts (e.g., photosynthetic carbon assimilation, carotenoid and chlorophyll biosynthesis), the function of most chloroplast proteins is not known.

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Chitnis and Rodermel have adopted a proteomics approach to identify novel thylakoid membrane proteins. Of ~150 proteins analyzed in a pilot study, 24% were derived from unidentified open reading frames. A holistic 'systems biology' approach involving mutational analysis and techniques of functional genomics will allow Chitnis and Rodermel to characterize the role of these proteins in photosynthesis.

Much of the regulatory traffic that coordinates gene expression in the chloroplast and nucleus is anterograde, i.e., from the nucleus to the plastid, in the form of nuclear gene products that control the transcription and translation of plastid genes (Rodermel, 2001). Among these products are sigma factors that regulate the activity of the plastid encoded RNA polymerase (PEP) (Allison, 2000). The Allison lab (NE-AES) has shown that two plastid-localized sigma factors are expressed differentially during the process of chloroplast biogenesis in maize (Lahiri and Allison, 2000). This is consistent with the idea that sigma factor families act as global regulators of plastid gene transcription.

In addition to anterograde traffic, retrograde traffic occurs between the plastid and nucleus in the form of “plastid signals” that regulate the transcription of nuclear genes for photosynthetic proteins (Rodermel, 2001). The Rodermel group (IA-AES) has used the immutans and var2 variegation mutants of Arabidopsis as models to understand these retrograde mechanisms. These mutants have green sectors with morphologically normal chloroplasts and white sectors with abnormal (non-pigmented) plastids that are blocked in the process of chloroplast biogenesis. Photosynthetic rates are markedly higher than normal in the green sectors of the mutants, and leaf morphogenesis is impaired in both, indicating a disruption in retrograde signaling (Aluru et al., 2001). Positional-cloning has revealed that IMMUTANS is a novel terminal oxidase that resides in the thylakoid membrane (Wu et al., 2000), and that VAR2 is a thylakoid membrane FtsH metalloprotease (Chen et al., 2000). Functional analyses of the IMMUTANS and VAR2 proteins by the Rodermel (IA-AES), Chitnis (IA-AES) and Daley (OR-AES) groups should lend insight into mechanisms of retrograde signaling, as well as provide information about factors that control photosynthetic rates.

Objective 2: Photosynthetic Capture and Photorespiratory Release of CO2

Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) initiates the major pathway of CO2 capture from the atmosphere by catalyzing the reaction between ribulose 1,5-bisphosphate (RuBP) and CO2 to produce two molecules of phosphoglycerate (Spreitzer, 1999). However, atmospheric O2 competes with CO2, and oxygenation of RuBP initiates the nonessential photorespiratory pathway that leads to the loss of CO2. Thus, if carboxylation could be increased or oxygenation decreased, a significant increase in crop plant productivity might be realized. Rubisco is comprised of eight 55-kD large subunits coded for by a single rbcL gene on the multicopy chloroplast DNA, and of eight 16-kD small subunits coded for by a family of RbcS genes in the nucleus. Because rbcL and RbcS are present in multiple copies per cell, it will be difficult to eliminate or transform engineered copies of these genes in crop plants. Despite these limitations, natural variation exists in the kinetic and regulatory properties of Rubisco from different species (Spreitzer, 1999), and thus it is possible that with advances in technology an improved higher plant enzyme might be created. For example, methods have been developed for engineering the small subunit by the Spreitzer group (NE-AES) (Spreitzer et

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al., 2001), and progress has been made with nuclear and chloroplast transformation of the green alga Chlamydomonas reinhardtii and of land plants by the Spreitzer groups and Allison (NE-AES) labs (Spreitzer, 1998; Daniell et al., 2002). These transformation technologies should provide new opportunities to study structure/function relationships of Rubisco. Many Rubisco X-ray crystal structures have now been solved that might also aid genetic engineering strategies (Taylor et al., 2002).

Modifications in the regulation of Rubisco might result in improved plant productivity, and models have been constructed that predict patterns of CO2 uptake by the Long (IL-AES) and Portis (IL-ARS) groups (Bernacchi et al., 2001). Rubisco activase enhances the activity of Rubisco by removing inhibitory sugar phosphates from the active site, and the Portis (IL-ARS) and Spretizer (NE-AES) groups have identified the site of interaction between activase and Rubisco (reviewed by Portis, 2001). The creation of transgenic plants with altered forms of Rubisco activase by the Portis group has shown that the amount and redox control of activase are important for growth (Zhang et al., 2001). However, increased knowledge of how activation varies in different plants is necessary for ultimately improving the regulatory mechanism. As another means of Rubisco regulation, enzymes involved in Rubisco modification have been characterized by the Houtz group (KY-AES) (Ying et al., 1999; Dirk et al., 2001); altered modification enzymes might prove to be appealing targets for genetic modification of crop plants if they result in more efficient carboxylation.

In C4 and Crassulacean (CAM) plants, phosphoenolpyruvate carboxylase (PEPC) catalyzes the initial fixation of atmospheric CO2 into C4-decarboxylic acids. Because this pathway concentrates CO2 in the vicinity of Rubisco, PEPC and its regulation are attractive targets for the genetic engineering of improvements in CO2 fixation. The Chollet (NE-AES) and Cushman (NV-AES) groups have shown that PEPC activity is tightly controlled by metabolites, as well as by reversible phosphorylation via PEPC kinase (PPcK) and protein phosphatase 2A (Vidal and Chollet, 1997; Taybi and Cushman, 1999). Molecular cloning of PPcK genes has allowed biochemical studies of the recombinant kinase and the development of immunological reagents for tracking its expression in various plant tissues. This work has increased our understanding of the regulation of PEPC in C/N partitioning and N2 fixation in legume nodules (Bakrim et al., 2001; Taybi et al., 2000). The Chollet group (NE-AES) has found that the chloroplast enzyme pyruvate orthophosphate dikinase (PPDK) is also controlled by phosphorylation in C4 and CAM photosynthesis (Chastain et al., 2000).

The mitochondrial pyruvate dehydrogenase complex (mtPDC) controls carbon flow from glycolysis to the Krebs cycle by catalyzing the oxidative decarboxylation of pyruvate to acetyl-CoA. The Randall group (MO-AES) has found that inhibition of the mtPDC by reversible phosphorylation might reduce CO2 release from respiration (Leuthy et al., 2001). Because the mitochondrial and chloroplast forms of PDC are involved in the generation of fatty acids (oil), further analysis of the mechanism of mtPDC phosphorylation might lead to the genetic engineering of value-added crops.

Objective 3: Mechanisms Regulating Photosynthate Partitioning

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Critical steps in the conversion of photosynthate to harvested materials can affect the photosynthetic process itself, as well as the amount of fixed carbohydrates allocated to yield. Key points in this regulation offer exciting avenues for manipulation; however, underlying mechanisms remain unclear. Feasible long-term targets for altered partitioning begin at the metabolic level (photosynthetic end-products) and extend to the whole plant level (importing plant parts). Recent work from NC-142 investigators and elsewhere indicate three especially promising avenues for regulation of photosynthate partitioning:

Sucrose biosynthesis and metabolism are key components of long-distance transport of photosynthates in vascular plants, and the extent of sucrose formation, metabolism, and sites of its conversion can markedly affect exporting and importing organs at many levels. Sucrose is typically synthesized in leaves via SPS (sucrose-P synthase) and cleaved at sites of import by either SuSy (sucrose synthase, a reversible reaction) or one of the invertases (in cell walls or vacuoles). Products of the invertase and SuSy paths differ (hexoses vs. fructose + UDPG), and so too does their potential to generate sugar signals. The Koch lab (FL-AES) has shown that these signals can repress genes for photosynthesis, and also affect invertase and SuSy genes themselves (Koch, 1996; Xu et al., 1996; Koch et al., 2000). In addition, sugar signals sensed through hexokinase can potentially be amplified by repeated cycles of sucrose cleavage and re-synthesis (Moore and Sheen, 1999; Rolland et al., 2001). Invertase action and the resulting signals are typically associated with growth, expansion and cell division, whereas SuSy is more often linked with biosynthesis of cell walls and storage materials (Sturm and Tang, 1999; Koch et al., 2000). SuSy also has broadly pleiotropic effects that include tuber yield and starch content in potato (Zrenner et al, 1995); flood tolerance in maize (Ricard et al., 1998; Zeng et al., 1998, 1999); fruit set under specific conditions in tomato (D’Aoust et al., 1999); and a critical, drought-sensitive step in N-fixing nodules of legumes (Arrese-Igor et al., 1999; Zhang et al., 1999); the Koch (FL-AES) and Chollet (NE-AES) groups have played seminal roles in these discoveries (Zeng et al., 1998, 1999; Zhang et al., 1999).

Invertase and SuSy regulation extends from transcriptional to post-transcriptional mechanisms. The Koch group (FL-AES) has found that transcription of genes for both enzymes responds strongly to sugars, oxygen status and other abiotic factors, and that both are also regulated at the level of mRNA stability (Koch, 1996; Xu et al, 1996; Zeng et al., 1999; Koch et al., 2000). The Huber (NC-AES) and Chollet (NE-AES) groups have found that SuSy proteins from both maize and soybean nodules can be phosphorylated at multiple sites; CDPKs and/or SnRKs have been implicated in these phosphorylation events (Huber et al., 1996; Zhang and Chollet, 1997; Nakai et al., 1998; Anguenot et al., 1999; Zhang et al., 1999).

Starch synthesis and degradation occur in chloroplasts of leaves and amyloplasts of non-green starch storage tissues (e.g., seeds and tubers). The extent of starch formation and use can be linked to both export and import of photosynthates by different plant parts. Starch is typically a composite of both amylose (unbranched α-l,4 glucan) and amylopectin (α-l,4 and α-1,6 branched glucan). Its synthesis requires three enzymes: AGP (ADP-glucose pyrophosphorylase), starch synthase, and BE (branching enzyme). In addition, a de-branching enzyme (Sugary-1 in maize) appears to be necessary for starch granule formation. AGP is an important regulatory enzyme and in many tissues it is activated by 3-P-glycerate and inhibited by inorganic phosphate. The Okita (WA-AES), Edwards (WA-AES) and Preiss (MI-AES) groups have analyzed the catalytic

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and regulatory sites of AGPs (Binderup et al., 2000; Frueauf et al., 2001; Sikka et al., 2001; Kavakli et al., 2001a; 2001b), and the Okita lab has found that starch content can be manipulated by altering the properties of AGP in transgenic plants (Slattery et al., 2000). The Preiss (MI-AES) and Guiltinen (PA-AES) labs have shown that starch quality depends on the properties of starch synthase and branching enzyme (Binderup et al., 2001; Blauth et al., 2001a, 2001b; Hong et al., 2001). Although little is known about the regulation of starch degradation, two amylolytic enzymes have been identified in chloroplasts of pea and Arabidopsis: one is an α-glucosidase and another is a Ca2+-independent α-amylase. The Duke group (WI-AES) has found that the latter enzyme might facilitate carbon export at night. A further understanding of the enzymes involved in starch metabolism might lead to strategies to manipulate starch quality or utilization.

Partitioning of photosynthates to sugar alcohols is a central feature of several plant species that shunt recently fixed C into acyclic polyols such as mannitol and sorbitol, or cyclitols such as ononitol. In addition to their transport and storage roles, the Bohnert (IL-AES) and Loescher (MI-AES) groups have shown that these assimilates might function as osmoprotectants for plants experiencing salt and water stress (Shen et al., 1997; Sheveleva et al., 1997; Gao and Loescher, 2000; Loescher and Everard, 2000). Stress-susceptible model or crop plants have been transformed with genes involved in the synthesis of these protectants by the Bohnert and Loescher labs, and while stress resistance is often observed, more detailed studies of the mechanisms are required.

Objective 4: Developmental and Environmental Limitations to Photosynthesis

Factors that enhance or limit agricultural productivity do so by impacting photosynthesis. Gains in yield of the major crops over the past half-century have been predominantly through improved harvest index (HI). HI has approached the maximum achievable for many crops, and future gains will depend on increasing total production. This, in turn, will depend on improving the efficiency of crop canopy light interception and utilization. It will therefore be important to maximize these efficiencies under optimal and stress conditions, consonant with global atmospheric change.

NC-142 collaborators have been active in a number of investigations that have explored developmental and environmental limitations to photosynthesis. These include nitrogen use, water use, stress (temperature, salt, drought, CO2), and developmental factors associated with canopy architecture and leaf ontogeny. Nitrogen acquisition and use is key to increasing actual efficiencies of light interception and use; improvements in nitrogen use efficiency (NUE) will also reduce the input of fertilizer needed for high yields. The Below group (IL-AES) has been studying the Illinois Protein Strains of maize --a germplasm with a wide range of NUEs—and found that little genetic variation exits for NUE in corn, probably because current hybrids have been selected under high N (Gentry et al., 2001). The Markwell group (NE-AES) has found that one-carbon metabolism plays a role in water-stress; they have focused on formate dehydrogenase as a means of increasing water use efficiency at the leaf level (Olson et al., 2000).

Stresses represent major limitations to photosynthesis and yield. The Jones group (MN-AES) has shown that maize kernel development is sensitive to heat stress during the first six days following pollination and is associated with decreased endogenous cytokinin levels

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(Commuri and Jones, 2001). Heat stress also disrupts amyloplast initiation, starch granule development, and storage protein levels. The Bohnert (IL-AES) and Cushman (NV-AES) groups have pioneered the use of microarrays, gene mining, and mutant analyses to investigate the mechanisms of drought and salt stress and the role of osmoprotectants in these processes (Cushman and Bohnert, 2000; Hasegawa et al., 2000).

Field studies of the effects of global change have scaled from photosynthetic processes to yield in two agricultural systems: increased N-deposition and drought in rangeland by the Knapp group (KS-AES) (Silletti and Knapp, 2001) and increased CO2 in soybean by the Long lab (IL-AES) (Hymus et al., 2001). Both showed changes in production anticipated from prior laboratory studies, but the mechanisms differed from expectations, emphasizing the importance of interaction between field and laboratory. For soybean, significantly increased canopy duration was a major factor, whereas for rangeland an increased contribution from the C4 photosynthetic component was a key factor.

Developmental factors also represent a major limitation to photosynthesis. For example, a model for light distribution within row-planted cotton canopies, based on the existing formulations for radiation transfer, has been integrated into a geometric model of the cotton canopy by the Sassenrath-Cole lab (MS-ARS). This model revealed that changes in leaf structure can enhance photosynthetic production. The Daley (OR-AES), Rodermel (IA-AES) and Edwards (WA-AES) groups have examined discontinuities in photosynthetic efficiency via fluorometry and found that these correlated with germplasm observations of dividing chloroplasts (Zheng et al., 2001a, 2001b). In addition it has been found that negative effects on photosynthesis attributed to environmental stresses are not only the direct result of decreases in photosynthesis but also a consequence of changes in plant development, e.g., that occur during the progression of leaf ontogeny (Rodermel, 1999).

OBJECTIVES

Objective 1 is to examine the dynamic regulation of radiant energy capture and utilization in photosynthesis, and to study the architecture, function and biogenesis of the photosynthetic apparatus.

Objective 2 is to determine and modify the biochemical and regulatory factors that impact the photosynthetic capture and photorespiratory release of CO2.

Objective 3 is to understand the mechanisms that regulate photosynthate partitioning into paths for biosynthesis and use of sucrose, starch, and sugar alcohols.

Objective 4 is to analyze the limitations and environmental factors that influence photosynthetic productivity at the whole plant and canopy levels.

METHODS

Objective 1: Photochemistry and the Biogenesis of the Photosynthetic Apparatus

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The Chitnis group (IA-AES) will generate cyanobacterial mutants to study structure-function relations in PSI. Specific objectives include a mutational analysis of the quinone redox center (A1 site) of PSI; a determination of how foreign quinones are recruited into the A1 site; and studies of the role of -carotene in excitation energy transfer in PSI. The Chitnis and Rodermel (IA-AES) groups will characterize mutants of Arabidopsis and cyanobacteria to understand mechanisms that control PSI and PSII stoichiometry. Daley (OR-AES) will perform fluorescence measurements to assess photosynthetic function in the mutants. The Chitnis and Rodermel groups will continue to define the thylakoid proteomes of cyanobacteria and plants. Proteins of unknown function will be characterized in knockout mutants using targeted mutagenesis of cyanobacteria and by screening T-DNA insertion populations of Arabidopsis. The mutants will be characterized in detail using global gene expression analysis techniques.

The role of sigma factors in chloroplast development will be studied by Allison (NE-AES) using RNAi technology and available T-DNA insertion (Arabidopsis) and Mu transposon-tagged (maize) lines. The consequences of sigma factor gene disruption will be analyzed by functional genomics approaches, including analyses of chloroplast gene chips probed with wild type versus mutant RNAs. In vivo promoter selection and promoter binding studies will also be conducted. Insight into retrograde signaling pathways and mechanisms of thylakoid membrane biogenesis will be studied by characterizing the immutans and var2 mutants of Arabidopsis. Techniques of proteomics and microarray analysis will be employed (Rodermel and Chitnis, IA-AES). Proteins that interact with IMMUTANS and VAR2 will be identified by gel filtration and co-immunoprecititation, by interaction cloning in yeast, and by generating second site suppressors. Photosynthesis in the mutants will be analyzed by Daley (OR-AES).

Objective 2. Photosynthetic Capture and Photorespiratory Release of CO2

By exploiting methods of chloroplast and nuclear transformation in Chlamydomonas, the Spretizer lab (NE-AES) will investigate the importance of large and small subunit residues that differ relative to those conserved in crop plant Rubisco enzymes. The Houtz group (KY-AES) will continue to define the biochemical significance of post-translational Rubisco methylations and hydroxylations and will exploit mutant Chlamydomonas enzymes that have been engineered by the Spreitzer group (NE-AES) to promote or block such modifications. By using tobacco chloroplast transformation, the KY-AES will also create amino acid substitutions to introduce post-translationally modified residues into crop plants; these studies will be performed in collaboration with the Allison group (NE-AES). The Portis group (IL-ARS) will attempt to extend chloroplast transformation technology to soybeans and replace endogenous Rubisco with the Chlamydomonas enzyme (via genes provided by the NE-AES), which has more favorable kinetic properties at high CO2. The Portis and Spreitzer labs will continue to collaborate on determining the structural basis for the interaction between Rubisco and Rubisco activase. A large-subunit loop that is known to influence this interaction will be replaced with the loop from crop plants. The Portis lab will also continue studies of the impact of transforming the rca mutant of Arabidopsis with mutant activase proteins that have altered catalytic and regulatory properties.

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The Chollet (NE-AES) and Cushman (NV-AES) groups will continue biochemical, molecular, and physiological investigations into the functional contribution and metabolic regulation of PEPC, PPcK, and PPDK. Because this research has direct relevance to regulatory protein phosphorylation in general, collaborations with the Randall (MO-AES), Portis (IL-ARS), and Huber (NC-ARS) groups are anticipated. The Chollet group will characterize the regulatory protein involved in the phosphorylation of PPDK, and begin to investigate divergent forms of PEPC as a means of gaining a deeper understanding of enzyme regulation. The Chollet and Cushman groups will expand their investigation of PPcK in C3, C4, and CAM plants by molecular and biochemical characterization of other isozymes. Investigations into the regulation and substrate specificity of PPcK and closely-related calcium-dependent protein kinases (CDPK) will be conducted in collaboration with the Huber group (NC-AES). CAM mutants of Mesembryanthemum crystallinum will be used to assess the molecular genetic, biochemical, and regulatory requirements for C4 metabolism by the Cushman group (NV-AES).

The Randall group (MO-AES) will define the biochemical and regulatory properties of the kinase that regulates the mitochondrial mtPDC. Knockout mutants of Arabidopsis that lack the regulatory kinase and phosphatase will be used to characterize mtPDC function in vivo. These mutants, as well as mtPDC mutants that lack the target residue for phosphorylation, will be characterized with respect to photosynthesis and evaluated for enhanced oil synthesis.

Objective 3: Mechanisms Regulating Photosynthate Partitioning

The steps involved in C-flow into and out of sucrose, starch, and sugar alcohols represent key points of control for photosynthate partitioning at the metabolic and whole plant levels. The proposed research will define mechanisms of regulation for each of these processes, and how they can be manipulated to increase productivity and yield.

Regulation of sucrose biosynthesis and metabolism will be approached in several ways. Regulation can be modulated in both exporting and importing tissues: for example, at points of sucrose formation via SPS (sucrose-P synthase) or cleavage by SuSy (sucrose synthase) or invertases (vacuolar and cell wall forms). To gain insight into mechanisms of sugar sensing, the Rodermel (IA-AES) and Moore (SC-AES) groups will use mutant and transgenic Arabidopsis with altered soluble invertase activities or with altered hexose sensing capacities. Both approaches should decrease hexose-based sugar signals. The impact of these alterations will be assessed by examining photosynthesis, plant development, diurnal carbohydrate profiles, and activities of cycling enzymes, and by conducting isotope assays of sucrose cycling. Invertase regulation and its role in development will be further examined using transgenic maize by the Koch (FL-AES), Jones (MN-AES) and Huber (NC-AES) groups. In these experiments (performed in collaboration with Pioneer Hi-Bred Int.), several types of transgenic lines will be generated: a) invertase promoter-GUS constructs for analysis of transcriptional control (FL-AES, NC-AES); b) lines that over-express soluble invertase in specific tissues to examine the developmental role of invertase (FL-AES); and c) lines in which cytokinin metabolism is altered to assess its impact in young kernels (MN-AES). A final regulatory aspect of sucrose metabolism that will be investigated is SuSy phosphorylation by the Koch (FL-AES), Chollet (NB-AES) and Huber (NC-AES) groups. Stable and transient expression approaches will be used to test functionality, localization, and substrate characteristics of non-phosphorylatable

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SuSy enzymes. Both maize and soybean will be utilized (vegetative and nodule tissues), together with antibodies to specific sites of SuSy phosphorylation. Of particular interest will be the identification of the effector kinase (a CDPK or SnRK).

Regulation of starch biosynthesis and degradation will include a major focus on AGP due to its central role in starch formation. One of the approaches will be to alter the regulatory properties of AGP by modifying the binding sites for 3-PGA activation or Pi inhibition. Ongoing work by the Preiss (MI-AES), Edwards (WA-AES) and Okita (WA-AES) groups indicates that inhibition of AGP by Pi might involve both N- and C-terminal domains of the protein; mutant proteins are being constructed to test this hypothesis. If these enzymes are less sensitive to Pi inhibition, or require less activator, they could be valuable resources for increasing starch and crop yields. The Preiss, Edwards and Okita groups will also test mutant AGP proteins for altered binding of the 3-PGA activator, and will evaluate the physiological effects of the mutant enzymes in transgenic plants (Arabidopsis, rice, and potato). In these studies, rice will serve as a model system, and mutant AGPs will be targeted to leaves, or to one of two compartments in cells of the seed endosperm (cytosol or amyloplasts). This approach will allow an independent assessment of the potential for starch storage in exporting versus importing tissues. Analyses will include measurements of seed weight, leaf and grain metabolites (hexoses, sucrose, and starch content), activity and content of key enzymes (e.g. AGP, Rubisco), leaf photosynthesis, and partitioning of radiolabeled photosynthates.

Another focus of research in this objective will be the molecular mechanisms regulating the activity of BE (branching enzyme). The Preiss group will utilize PCR random mutagenesis to alter BE structure and properties, whereas the Edwards and Okita groups will use Mu insertional mutants to study effects of altered BE enzymes in vivo and in vitro. The Duke group (WI-AES) will study the regulation of starch degradation by generating Arabidopsis mutants with defects in the chloroplast α-glucosidase and Ca2+-independent α-amylase; the mutants will be examined using procedures similar to those discussed above for the AGP mutants.

The role of polyol sugars in imparting protection from drought or salt stress will be studied by the Bohnert (IL-AES) and Loescher (MI-AES) groups using stable transgenic model and crop plants. Photosynthetic characteristics of transformed tobacco and Arabidopsis plants producing mannitol, sorbitol, or ononitol will be assessed after salt stress. The importance of having cytosolic or chloroplastic polyols will be examined further. These experiments will define the protective characteristics of each polyol and the preferred compartment for its synthesis and accumulation, thereby providing insights into the use of polyols for engineering stress tolerance (see Objective 4). Recent progress in regeneration and transformation of celery (a mannitol syntheziser) and cherry (a sorbitol synthesizer) by the Loescher group (MI-AES) will allow study of genetically modified polyol biosynthesis.

Objective 4: Developmental and Environmental Limitations to Photosynthesis

NC-142 collaborators will focus on the impact of six major developmental and environmental limitations to photosynthesis:

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1. Nitrogen use. Physiological components of NUE will be determined by the Below group (IL-AES) in field trials of different genotype x N rate treatments using resources of the Illinois Protein Strains of maize. In addition to physiological studies, the plant samples will be assayed for changes in the expression of genes known to be involved in nitrogen metabolism and storage product deposition. The NE-AES (Markwell group) will determine whether the expression of uricase, which is essential for mobilization of fixed N2, might be used as a QTL marker in different soybean breeding lines.

2. Temperature stress. The Knapp group (IA-AES) will study the effects of low temperature stress on photosynthesis and yield using a range of maize genotypes that differ in their tolerance to low temperature. The transition of seedlings from heterotrophic to autotrophic growth will be characterized and genotypes screened for photosynthetic competence. The Knapp (IA-AES) and Jones (MN-AES) groups will compare tolerance to low and high temperature stresses. The Chitnis group (IA-AES) will characterize the proteomes of the stressed plants to identify proteins that might be targeted for genetic manipulation.

3. CO2 and ozone stress. Field studies of the impacts of global change on photosynthetic production will be expanded by the Long (IL-AES) and Knapp (KS-AES) groups. Tropospheric ozone is thought to account for $6 billion of crop losses in the US, and its continued rate of increase might eliminate any increase in production due to rising CO2. The new Free-Air Concentration Enrichment experiment (SoyFACE) will add ozone (1.5x ambient) to its elevated CO2 treatment (1.5x ambient). This will be the first field system worldwide that simultaneously treats crops in the open air with both ozone and CO2 elevated to predicted future levels. This is a resource that will be used by other NC-142 participants. For example, the Rodermel group (IA-AES) will use proteomics to characterize changes in expressed polypeptides. The KS-AES (Knapp) will conduct parallel studies of global change effects on rangeland, focusing on increased N-deposition and drought incidence.

4. Photosynthetic limitations in canopies. Cotton will be used as a model system. Monitoring crop performance on the broad scale required of production agriculture is challenging, tedious, and error-prone. Within-field spatial variability affects canopy microclimate, crop growth, cotton fiber development, and final fiber quality and yield, and can cause significant reductions in the net return to farmers. The Sassenrath-Cole group (MS-ARS) will explore edaphic x microclimate effects on cotton production systems. Photosynthetic limitations in canopies will be assessed via geometric models of canopy structure, radiation transfer, and microclimate.

5. Salt and drought stress response. The role of signal transduction in stress sensing and tolerance responses will be studied by the Bohnert group (IL-AES). Transcriptional and post-translational responses in gene regulation to varied salt concentrations will be determined. Collaborative studies with the Cushman group (NV-AES) will elucidate the physiological aspects of salt and drought tolerance in whole plants, and both groups will undertake mechanistic studies that involve genome-wide transcript expression profiles (microarrays), gene mining, and mutant analyses (see Cushman and Bohnert, 2000).

6. Water-use efficiency. The Markwell group (NE-AES) will examine whether altering one-carbon metabolism by overexpressing formate dehydrogenase in transgenic tobacco alters water-

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use efficiency. Plants with 25 to 50-fold elevated levels of the enzyme will be grown under water-sufficient and –deficient conditions and WUE will be assess by 13C-isotope ratio mass spectrometry.

In addition to these six major initiatives, other NC-142 participants will contribute to this objective, but in more limited ways. For example, the impact of taxol on photosynthesis and plant development will be assessed by the Daley group (OR-AES). The IA-AES (Rodermel group) will also use antisense Rubisco mutants to assess the impact of Rubisco on photosynthesis and plant growth, and variegation mutants to understand developmental effects on photosynthesis.

MEASUREMENT OF PROGRESS AND RESULTS

Objective 1: Photochemistry and the Biogenesis of the Photosynthetic Apparatus

a. OutputsThe features of quinones and of quinone-binding sites that are essential for their function as

redox centers in PSI will be determined (IA-AES). Mechanisms that control PSI and PSII stoichiometry will be identified (IA-AES, OR-AES). A map of the thylakoid proteome will be expanded and novel proteins characterized (IA-AES).Plastid transcripts that are expressed in different tissues and under different growth conditions

will be identified (NE-AES). Components of plastid-to-nucleus signal transduction pathways and of thylakoid membrane

biogenesis will be clarified (IA-AES, OR-AES).

b. Outcomes and Projected ImpactsIt might be possible to design strategies to generate plants with improved photosynthetic

performance and yield, or with value-added traits, with an improved understanding of 1) the function of PSI redox centers; 2) the regulation of PSI/PSII stoichiometry; 3) the mechanisms that control thylakoid complex assembly; 4) the function of novel thylakoid proteins; and 5) transcription mechanisms in plastids (IA-AES, NE-AES, OR-AES).

c. MilestonesCyanobacterial mutants will need to be generated by years 1 and 2 to study structure-function

relationships in PSI and to study the regulation of photosystem stoichiometry (IA-AES). Knockout and RNAi mutants will need to be produced in years 1, 2 and 3 in genes for novel

thylakoid proteins in cyanobacteria and plants, and for sigma factor genes in maize and Arabidopsis (IA-AE, NE-AES).

Objective 2. Photosynthetic Capture and Photorespiratory Release of CO2

a. OutputsThe role of the Rubisco small subunit in determining Rubisco catalytic efficiency will be

elucidated (NE-AES).Enzymes, mechanisms, and the significance of Rubisco post-translational modifications will be

defined with respect to Rubisco synthesis, structure, and function (KY-AES, NE-AES).

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Structural interactions between Rubisco and Rubisco activase will be established with respect to both proteins (IL-ARS, NE-AES).

Mutant forms of Rubisco activase will be created in vivo for physiological studies (IL-ARS).Signal transduction pathways for the regulatory phosphorylation of enzymes involved in C4 and

CAM metabolism will be elucidated (NE-AES, NV-AES, NC-AES).The function of PPcK will be examined in transgenic C3/C4 and CAM model species (NV-AES,

NE-AES).A collection of CAM-deficient mutants will be created (NV-AES).The function of the mtPDC and its associated regulatory proteins will be examined in transgenic

C3 model species (MO-AES, NE-AES, NV-AES, NC-AES).Knockout mutants of Arabidopsis will be isolated and evaluated for increased carbohydrate and

oil composition (MO-AES).

b. Outcomes and Projected ImpactsGenetic engineering of the Rubisco small subunit, post-translational modifications, and/or

interactions with Rubisco activase might increase carboxylation efficiency and crop plant productivity (NE-AES, KY-AES, IL-ARS).

A deeper knowledge of regulatory phosphorylation and PEPC structure/function relationships in C4 and CAM plants might allow CO2 concentrating mechanisms to be genetically improved or transferred to C3 crop plants (NE-AES, NV-AES).

Genetic engineering of the mtPDC and its associated mechanisms of regulation might reduce the loss of CO2 and increase oil production (MO-AES).

c. MilestonesTransformation of genetically-engineered rbcL genes into tobacco (NE-AES) will be required by

year 2 to provide material for studies on Rubisco post-translational methylation (KY-AES). Directed mutants of Chlamydomonas Rubisco will need to be generated in the Rubisco activase

binding region via chloroplast transformation (NE-AES) by year 3 and analyzed for effects on activation efficiency (IL-ARS).

The gene encoding the regulatory protein of PPDK will need to be cloned by year 2 as a means for defining the biochemistry of regulatory phosphorylation (NE-AES).

CAM mutants of Mesembryanthemum crystallinum will need to be generated by years 1 through 4 (NV-AES) for use in analyzing C4 (NE-AES, NV-AES) and starch (MI-AES, PA-AES) metabolism.

Arabidopsis knockout mutants will need to be identified by year 2 for subsequent use in the study of mtPDC regulatory phosphorylation (MO-AES).

Objective 3: Mechanisms Regulating Photosynthate Partitioning

a. Outputs Transgenic Arabidopsis with altered soluble invertase activity will be generated (IA-AES).Transgenic maize with altered genes for invertases (FL-AES), cytokinin oxidase (MN-AES), and

sucrose synthase will be generated (Fl-AES, NC-AES).Antibodies to specific forms of phosphorylated forms of sucrose synthase from maize (NC-AES)

and soybean will be produced (NB-AES).

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Transgenic Arabidopsis and rice plants with altered AGP and starch storage capacity in leaves and seeds will be generated (WA-AES).

Maize mutants will be created with altered genes for BE and starch quality (PA-AES).Modified genes for AGP with regulatory properties that facilitate greater starch production will

be produced (MI-AES, WA-AES).Modified genes for BE that allow analysis of its regulation and control of starch quality will be

generated (MI-AES, PA-AES).Structural information will be produced on genes for starch biosynthesis that allows further

regulatory control. Polyol transporters for sorbitol and mannitol will be identified.

b. Outcomes and Projected ImpactsData will show whether sucrose cycling can affect signals to sugar-responsive genes (SC-AES).Results will define transcriptional regulation of soluble invertase in maize, its impact on kernel

development, and the role of cytokinin metabolism in import by young kernels (FL-AES, MN-AES).

Information will determine roles and regulation of SuSy phosphorylation as well as the kinases involved (FL-AES, NB-AES, NC-AES). Localization and activity of SuSy could markedly affect sucrose use in many plant parts, and provide a valuable tool for its manipulation.

Collectively, the above will enhance understanding of the molecular mechanisms for photosynthate partitioning, and could profoundly affect approaches to yield improvement.

Information and materials from the molecular to whole-plant levels will allow starch storage and yield to be increased through control of AGP.

Molecular information and mutant plants will facilitate the first steps toward manipulation of starch quality through regulation of BE.

Definition of starch breakdown mechanisms could provide new means of controlling its storage, and determine a role for a potentially valuable, but enigmatic enzyme ( amylase).

Crop plants with substantial improvements in productivity and stress tolerance will be generated (IL-AES, MI-AES).

c. MilestonesProduction of necessary transgenic Arabidopsis plants will need to be competed within the first

year, and their initial characterization should be finished within the following two years.Transgenic maize materials should be ready for testing after the second year. Antibodies to specific phosphorylated forms of SuSy will be available within the first year.Transgenic Arabidopsis with altered AGP will need to be generated within the first year.Transgenic rice with new constructs should be available after the second year.Crystal structure of AGP should be more fully defined within 2 to 3 years.Transgenic Arabidopsis with altered capacity for polyol biosynthesis will be generated within

the first year, and these will then be used to analyze both primary and secondary effects of these biosynthetic genes in photosynthesis, partitioning, and stress tolerance.

Objective 4: Developmental and Environmental Limitations to Photosynthesis

Outputs

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Improved models for optimizing light distribution in cotton canopies will be defined (MS-ARS).The role of endogenous cytokinin production in temperature response of early kernel filling in

corn will be established (MN-AES).Genes or pathways will be discovered that are associated with or that potentially regulate NUE,

storage product deposition, and salinity tolerance (IL-AES, NV-AES).Genotypes, including growth forms, will be identified that have increased yields under

atmospheric change (IL-AES, KS-AES).The role of taxol in photosynthesis and plant development will be established (OR-AES).The significance of uricase in mobilization of fixed N2 in soybean will be established (NE-AES).The role of C-1 metabolism in photosynthetic efficiency will be elucidated (NE-AES).

b. Outcomes and Projected ImpactsGermplasm will be developed with increased photosynthetic potential under elevated CO2 and

ozone for use in breeding programs (IL-AES).Corn germplasm will be developed for increased NUE that might save growers money spent on

N fertilizer and decrease N runoff (IL-AES).The uricase gene will be developed as a QTL marker in soybean selection (NE-ARS).New criteria will be established for selection of canopy properties in cotton breeding (MS-ARS).

c. MilestonesFree-air concentration enrichment will need to be developed by year 2, constructed, and

deployed for controlled increase in ozone within soybean in the open-air (IL-AES).Three years of trials and analysis of the effects of elevated CO2 and two of ozone on soybean

photosynthetic production will need to be completed (IL-AES).

PROJECTED PARTICIPATION: APPENDIX 4, APPENDIX 5, AND APPENDIX E-1

OUTREACH PLAN

The major advances and discoveries of the proposed research will be published in scientific journals and meeting proceedings. Peer-reviewed publication is the best practical method for evaluating the quality and impact of the research results. NC-142 investigators have been successful in this endeavor, as illustrated by the large number of articles published by the groups members in high impact, high quality journals (See APPENDIX 2). Research results will also be presented as platform lectures and poster presentations at local, regional, national, and international scientific meetings. NC-142 collaborators have also been successful in this arena, delivering many high profile presentations (See APPENDIX 3).

As another outreach effort, field days will be organized at the SoyFACE facility for commodity/grower groups to explain the facility and results, both state and national, via the National Soybean Research Laboratory and soybean commodity groups. An annual field day will also be held for grower groups to show progress in selection of improved NUE (IL-AES). Finally, an NC-142 website will be established for information exchange among collaborators and for dissemination of research results to the public.

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ORGANIZATION AND GOVERNANCE: Standard

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Bakrim N, Brulfert J, Vidal J, Chollet R (2001) Phosphoenolpyruvate carboxylase kinase is controlled by a similar signaling cascade in CAM and C4 plants. Biochem Biophys Res Commun 286: 1158-1162

Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR Jr, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24: 253-259

Binderup K, Watanabe L, Polikarpov I, Preiss J, Arni RK (2000) Crystalization and preliminary X-ray diffraction analysis of the catalytic subunit of ADP-glucose pyrophosphorylase from potato tuber. Acta Crystalographica D56:192-194

Binderup K, Mikkelsen R, Preiss J (2001) Truncation of the amino-terminus of branching enzyme changes branching pattern. Arch Biochem Biophys (In press)

Blauth SL, Klucinec J, Yao Y, Shannon JC, Thompson DP, Guiltinen MJ (2001a) Identification of Mutator insertional mutants of starch branching enzyme 2a (Sbe2a) in Zea mays L. Plant Physiol 125:1396-1405

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APPENDIX 2: SELECTED PUBLICATIONS OF NC-142 PARTICIPANTS FROM THE LAST PROJECT PERIOD

Abad MC, Binderup K, Preiss J, Geiger JH (2002) Crystallization and preliminary X-ray diffraction studies of Escherichia coli Branching Enzyme. Acta Crystallographica D series, in press.

Adam Z, Adamska I, Nakabayashi K, Ostersetzer O, Haussuhl K, Manuell A, Zheng B, Vallon O, Rodermel SR, Shinozaki K, Clarke AK (2001) Chloroplast and mitochondrial proteases in Arabidopsis thaliana: a proposed nomenclature. Plant Physiol 125: 1912-1918

Aguilera C, Stirling CM, Long SP (1999) Genotypic variation within Zea mays for susceptibility to and rate of recovery from chill-induced photoinhibition of photosynthesis. Physiol Plant 106: 429-436

Allison LA (2000) The role of sigma factors in plastid transcription. Biochimie 82: 537-548Allison LA, Simon LE, Maliga P (1996) Deletion of rpoB reveals a second distinct transcription system in plastids

of higher plants. EMBO J 15: 2802-2809Aluru M, Bae H, Wu D, Rodermel S (2001) The Arabidopsis immutans mutation affects plastid differentiation and

the morphogenesis of white and green sectors in variegated plants. Plant Physiol 127: 67-77Armbrust TS, Chitnis PR, Guikema JA (1996) Organization of photosystem I polypeptides examined by chemical

cross-linking. Plant Physiol 111: 1307-1312Athwal GS, Huber JL, Huber SC (1998) Phosphorylated nitrate reductase and 14-3-3 proteins: the site of

interaction, effects of ions, and evidence for an AMP binding site on 14-3-3 proteins. Plant Physiol 118: 1041-48

Athwal GS, Huber JL, Huber SC (1998) Biological significance of divalent cation binding to 14-3-3 proteins in relationship to nitrate reductase inactivation. Plant Cell Physiol 39: 1065-1072

Athwal GS, Huber SC (200X). Divalent cations and polyamines bind to loop 8 of 14-3-3 proteins, modulating their interaction with phosphorylated nitrate reductase. Plant J, in press

Athwal GS, Lombardo CR, Huber JL, Masters SC, Fu H, Huber SC (2000) Modulation of 14-3-3 protein interactions with target polypeptides by physical and metabolic effectors. Plant Cell Physiol 41: 523-533

Bachmann M, Huber JL, Liao P-C, Gage DA, Huber SC (1996) The inhibitor protein of phosphorylated nitrate reductase from spinach (Spinacia oleracea L.) leaves is a 14-3-3 protein. FEBS Letters 387: 127-131

Bachmann M, Huber JL, Athwal GS, Wu K, Ferl RJ, Huber SC (1996) 14-3-3 proteins associate with the regulatory phosphorylation site of spinach leaf nitrate reductase in an isoform-specific manner and reduce dephosphorylation by endogenous protein phosphatases. FEBS Lett 398: 26-30

Bachmann M, Shiraishi N, Campbell WH, Yoo B-C, Harmon A, Huber SC (1996) Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase. Plant Cell 8: 505-517

Bakrim N, Brulfert J, Vidal J, Chollet R (2001) Phosphoenolpyruvate carboxylase kinase is controlled by a similar signaling cascade in CAM and C4 plants. Biochem Biophys Res Commun 286: 1158-1162

Ballicora MA, Freuauf JB, Fu Y, Schürmann P, Preiss J, (2000) Activation of the potato tuber ADP-glucose pyrophosphorylase by thioredoxin. J Biol Chem 275: 1315-1320

Ballicora MA, Fu Y, Frueauf JB, Preiss J (1999) Heat stability of the potato tuber ADP-glucose pyrophosphorylase. Role of Cys residue 12 in the small subunit. Biochem Biophys Res Commun 257: 782-786

Ballicora MA, Fu Y, Nesbitt NM, Preiss J (1998) ADP-glucose pyrophosphorylase from potato tuber. Site-directed mutagenesis studies of the regulatory sites. Plant Physiol 118: 265-274

Barkla BJ, Vera-Estrella R, Kirch H-H, Pantoja O, Bohnert HJ (1999) Aquaporin localization – how valid are the TIP and PIP labels? Trends Plant Sci 4: 86-88

Bassman JH, Robberecht R, Edwards GE (2001) Effects of enhanced UV-B radiation on growth and gas exchange in Populus deltoides Bartr. Ex Marsh. Int J Plant Sci 162: 103-110

Bassman JH, Edwards GE, Robberecht R. (200X) Effects of long-term exposure to enhance UV-B radiation on growth and gas exchange in Pseudotsuga menziesii. New Phytol: in press

Baum TJ, Wubben MJE, Hardy KA, Su H, Rodermel SR (2000) A screen for Arabidopsis thaliana mutants with altered susceptibility to Heterodera schachtii. J Nematology 32: 166-173

Beale CV, Bint DA, Long SP (1996) Leaf photosynthesis in the C-4-grass Miscanthus x giganteus, growing in the cool temperate climate of southern England. J Exp Bot 47: 267-273

Beale CV, Long SP (1997) Seasonal dynamics of nutrient accumulation and partitioning in the perennial C-4-grasses Miscanthus x giganteus and Spartina cynosuroides. Biomass Bioenergy 12: 419-428

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Beale CV, Morison JIL, Long SP (1999) Water use efficiency of C-4 perennial grasses in a temperate climate. Agric Forest Meteor 96: 103-115

Beardslee T, Chowdhury SR, Chang CC, Jaiswal P, Buhot L, Lerbs-Mache S, Stern DB, Allison LA (200X) A nuclear-encoded maize protein with sigma factor activity is targeted to both chloroplasts and mitochondria. submitted to Plant Physiology

Beardslee TA, Zeece MG, Sarath G, Markwell JP (2000) Soybean glycinin G1 acidic chain shares IgE epitopes with peanut allergen Ara h 3. Int Arch Aller Immunol 123: 299-307

Below FE, Cazetta JO, Seebauer, JR (2000) Carbon/nitrogen interactions during ear and kernel development of maize. In M Westgate, K Boote, eds, Physiology and modeling kernel set in maize. CSSA Spec Publ 29. CSSA, Madison WI, p 15-24

Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP (2001) Improved temperature response functions for models of Rubisco- limited photosynthesis. Plant Cell Environ 24: 253-259

Binderup K, Libessart N, Preiss J (2000) Slow-binding inhibition of branching enzyme by the pseudo-oligosaccharide BAY e4609. Arch Biochem Biophys I374: 73-78

Binderup K, Mikkelsen R, Preiss J (2000) Limited proteolysis of branching enzyme from Escherichia coli. Arch Biochem Biophys 377: 366-371

Binderup K, Mikkelsen R, Preiss J (2001) Truncation of the amino-terminus of Branching Enzyme changes in branching Pattern. Arch Biochem Biophys, in press

Binderup K, Preiss J (1998) Glutamine-459 is important for Escherichia coli branching enzyme activity. Biochemistry 37: 9033-9037

Binderup K, Watanabe L, Polikarpov I, Preiss J, Arni RK (2000) Crystallization and preliminary X-ray diffraction analysis of the catalytic subunit of ADP-glucose pyrophosphorylase from potato tuber. Acta Crystallographica D56: 192-194

Blauth SL, Klucinec J, Shannon JC, Thompson DB, Guiltinan MJ (2001) Identification of Mutator insertional mutants of starch branching enzyme 2a (Sbe2a) in Zea mays L. Plant Physiol 125: 1396-1405

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Zeng Y, Wu Y, Avigne WT, Koch KE (1999) Rapid repression of maize invertases by low oxygen: Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Plant Physiol 121: 599-608

Zhang XQ, Chollet R (1997) Phosphoenolpyruvate carboxylase protein kinase from soybean root nodules: Partial purification, characterization, and up/down-regulation by photosynthate supply from the shoots. Arch Biochem Biophys 343: 260-268

Zhang XQ, Chollet R (1997) Seryl-phosphorylation of soybean nodule sucrose synthase (nodulin-100) by a Ca2+-dependent protein kinase. FEBS Lett 410: 126-130

Zhang X-Q, Lund AA, Sarath G, Cerny RL, Roberts DM, Chollet R (1999) Soybean nodule sucrose synthase (nodulin-100): Further analysis of its phosphorylation using recombinant and authentic root-nodule enzymes. Arch Biochem Biophys 371: 70-82

Zhang X-Q, Verma DPS, Patil S, Arredondo-Peter R, Miao G-H, Kuismanen R, Klucas RV, Chollet R. (1997) Cloning of a full-length sucrose synthase cDNA from soybean (Glycine max) root nodules (Accession No. AF030231) (PGR 97-173). Plant Physiol 115: 1729

Zheng P, Ammar K, Girard AM, Wetzel C, Rodermel S, Thomas DR, Ning L, Callis JB, Edwards GE, Daley L (2001) Tests of in vivo method to detect chloroplast division in crop plants: Part 1. Discovery of the phenomena. Spectroscopy (accepted).

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Zheng P, Ammar K, Girard AM, Wetzel C, Rodermel S, Thomas DR, Ning L, Callis JB, Edwards GE, Daley L (2001) Tests of in vivo method to detect chloroplast division in crop plants: Part 2. Verification of phenomena by germplasm methods and confocal microscopy. Spectroscopy (accepted)

Zheng Q, Simel EJ, Klein PE, Royer MT, Houtz RL (1998) Expression, purification, and characterization of recombinant ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit ?N-methyltransferase. Prot Exp Purif 14: 104-112

Zhu G, Bohnert HJ, Jensen RG, Wildner GF (1998) Formation of the tight-binding inhibitor, 3-ketoarabinitol-1,5-bisphosphate by ribulose-1,5-bisphosphate carboxylase/oxygenase is 02 dependent. Photosyn Res 55: 67-74

Zhu G, Jensen RG, Bohnert HJ, Wildner GF, Schlitter GF (1998) Dependence of catalysis and C02/02 specificity of Rubisco on the carboxy-terminus of its large subunit. Photosyn Res 57: 71-79

Zybailov B, Shen G, Vassiliev I, Reatégui R, Johnson W, Xu W, Chitnis PR, Golbeck JH (1998) Mutants in the menA and menB biosynthetic pathway: Photosystem I recruits a foreign quinone into the A1 binding site. In J Garab, ed, Photosynthesis: Mechanisms and Effects. Dodrecht: Kluwer Academic, pp 647-650

Zybailov B, van der Est A, Zech SG, Teutloff C, Johnson TW, Shen G, Bittl R, Stehlik D, Chitnis PR, Golbeck JH (2000) Recruitment of a foreign quinone into the A(1) site of photosystem I. II. Structural and functional characterization of phylloquinone biosynthetic pathway mutants by electron paramagnetic resonance and electron-nuclear double resonance spectroscopy. J Biol Chem 275: 8531-9

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APPENDIX 3: SELECTED PRESENTATIONS OF NC-142 PARTICIPANT SINCE 1999

Allison, L., Research seminar, Biology Division, Kansas State University, 1999.

Allison, L., Research seminar, Department of Molecular Biology, University of Wyoming, 1999.

Allison, L., Research seminar, Integrative Photosynthesis Research Group, University of Illinois, 2000.

Allison, L. Research seminar, Div.of Biological Sciences, Univ of Missouri-Columbia, 2000.

Below, F.E. (2000) Invited research presentation, ASA meetings, 2000.

Bohnert, H.J., Symposium speaker, 3rd Internatl Crop Sci. Conference, Hamburg, Germany, 2000.

Bohnert, H.J., Research presentation, NSF, Plant Genome meeting, Arlington, VA, 2000.

Bohnert, H.J.,-Research presentation, SFB Meeting "Plant interactions with the Environment", Retzbach, Germany, 2000.

Bohnert, H.J., Symposium speaker, "Rice Genome" Internatl Conference, IRRI, Los Baños, Philippines, 2000.

Bohnert, H.J., Research presentation, Plant Genome meeting, San Diego, CA, 2001.

Bohnert, H.J., Symposium speaker, International Congress "Plant Nutrition", Amsterdam, Netherlands, 2001.

Bohnert, H.J., Research presentation, Italian Agronomical Society, Salsomaggiore, 2001.

Bohnert, H.J., Research presentation, Workshop "Plant Ion & Metabolite Transport" Barcelona, Spain, 2001.

Bohnert, H.J., Symposium speaker, Interntl Symposium on Plant Environment Interactions, Taipei, Taiwan, 2001.

Chollet, R., Research-seminar, Institut de Biotechnologie des Plantes, Université Paris-Sud, Orsay, France, 2001.

Chollet, R., Research-seminar, Yield Enhancement Group at the Monsanto Company in St. Louis, MO., 2001.

Chollet, R.,Research-seminar, Department of Biochemistry at the Universityof Missouri-Columbia, 2001.

Chollet, R., Chair of the Discussion Session on “Phosphospecific Antibodies” at the Plant Protein Phosphorylation Workshop in Tahoe City, CA, 2001.

Chollet, R., Co-Chair of the Discussion Session on “Phosphorylation-Site Mapping” at the Plant Protein Phosphorylation Workshop in Tahoe City, CA, 2001.

Chollet, R., Invited speaker and session co-chair in the international symposium on “Photosynthetic CO2-Assimilating Enzymes: RuBisCO and PEPC”, Hyogo, Japan, 2000.

Chollet, R., Speaker in the international symposium on “Plant Protein Phosphorylation - Dephosphorylation” at the University of Missouri-Columbia 2000.

Chollet, R., Two research-seminars presented in the Division of Integrated Life Science/Graduate School of Biostudies and the Wood Research Institute of Kyoto University, Japan, 2000.

Chollet, R., Research-seminar, Department of Plant & Microbial Biology at the University of California-Berkeley, 2000.

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Cushman, J.C., Organizer Nevada EPSCoR Genomics Scientific Conference/Research Seminar on “Functional Genomics of Plant Abiotic Stress Tolerance” Lake Tahoe, NV, 2001.

Cushman, J.C., Symposium speaker, 12th International Congress on Photosynthesis. Brisbane, Australia, 2001.

Cushman, J.C., Symposium speaker, 3rd International CAM Congress, Coconut Beach Resort, Queensland, Australia, 2001.

Cushman, J.C., Research seminar on “Osmoregulation in Plants” Ann. Meeting of Society for Comparative and Integrative Biology, Atlanta, GA, 2000.

Cushman, J.C., Research seminar, Department of Botany, Iowa State University, Ames IA, 2000.

Cushman, J.C., Research seminar, Department of Botany and Microbiology, University of Oklahoma, Norman, OK, 2000.

Cushman, J.C., Research seminar, Div. of Plant Biology, S.R. Noble Foundation, Ardmore, OK, 2000.

Cushman, J.C., Two research seminars, University of Technology, Darmstadt. Graduierten kolleg 340, Riezlern, Austria, 2000.

Cushman, J.C., Research seminar, University of Illinois, Champaign-Urbana, 2000.

Edwards, G.E. Two seminars, Biochemistry Department, University of Rosario, Argentina, 2000

Edwards, G.E. Symposium chair, Symposium on “C4 Photosynthesis” at the 12th International Congress on Photosynthesis, Brisbane, Australia. 2001

Edwards, G.E. Symposium speaker, 11th Western Photosynthesis Conference, Asilomar, California, 2002

Guiltinan, M. J., Research seminar, Intercollege Program in Plant Physiology Seminar Series, University Park, PA, 2000

Guiltinan, M. J., Research seminar, Hershey Corporate Center, Hershey, PA, 2000

Guiltinan, M. J., Research seminar, Dept. of Biology and Dept. of Environmental Resources, Texas A&M University, College Station, TX, 2000

Guiltinan, M. J., Research seminar, Penn State Agricultural Council, University Park, PA, 2000

Guiltinan, M. J., Research seminar, 13th International Cocoa Conference, Kuala Lumpur, Malaysia, 2000

Guiltinan, M. J., Research seminar, Purdue University, 2001

Guiltinan, M. J., Research seminar, University of Maryland, College Park, MD, 2001

Guiltinan, M. J., Research seminar, USDA, Beltsville, MD, 2001

Guiltinan, M. J., Research seminar, Iowa State University, 2001

Houtz, R.L., Invited research presentation, NIAR/COE/BRAIN-RITE International Symposium on “Photosynthetic CO2-Assimilating Enzymes: Rubisco and PEPC”, Hyogo, Japan, 2000.

Houtz, R.L. Invited Member, Scientific Advisory Board, 5 th International Conference on the Role of Formaldehyde in Biological Systems B Methylation and Demethylation Processes, Sopron, Hungary, 2000.

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Houtz. R.L., Invited Speaker, 6th International Congress on Amino Acids, Bonn, Federal Republic of Germany, 1999.

Huber, SC, Symposium presentation, Annual Meeting of the Japanese Society of Plant Physiologists, 2000.

Huber, S.C., Session chair and symposium presentation, ‘Current Topics in Plant Biochemistry, Physiology and Molecular Biology’ Annual Symposium at the University of Missouri, 2000.

Huber, S.C., Symposium presentation, Wallenfels International Photosynthesis Conference, 2000.

Huber, S.C., Symposium presentation, Plant Biochemistry and Molecular Biology Conference on ‘Biosynthesis of Glucose Polysaccharides’ at Iowa State University, 2000.

Huber, S.C., Symposium presentation, First International Plant 14-3-3 Workshop at Roskilde, Denmark, 2000.

Huber, S.C., Symposium presentation, Final Symposium of SFB 251 ‘Ecology, Physiology and Biochemistry of Plants and Animals Under Stress’ University of Wuerzburg, Germany, 2000.

Huber, S.C., Research seminar, University of Goettingen, 2000.

Huber, S.C., Symposium presentation, Cold Spring Harbor Conference on ‘Sugar Sensing and Signaling in Plants and Other Organisms,’ 2000.

Huber, S.C., Session chair and symposium presentation at PS2001, 12th International Congress on Photosynthesis, Brisbane, Australia, 2001.

Knapp, A.D. Invited Research presentation, Joint Meetings, Society for Range Management and American Forage and Grassland Council, Omaha NE, 1999.

Knapp A.K., Research seminar, Department of Plant Biology, Arizona State University , 2000

Knapp A.K., Research seminar, Department of Botany and Microbiology, University of Oklahoma, 2000.

Knapp A.K., Research seminar, Kruger National Park, Skukuza, South Africa, 2000.

Knapp A.K., Research seminar, Department of Ecology and Evolution, Rice University, 2001.

Knapp A.K., Research seminar, Natural Sciences Convocation, McPherson College, McPherson, KS, 2001.

Koch, K.E., Symposium speaker, Nalbandov Symposium on Plant Responses to Global Climate Change, Champaign-Urbana, IL , 2001

Koch, K.E., Research presentation, Washington State University- National Biochemistry Training Program, Pullman, WA, 2001

Koch, K.E., Symposium speaker, Canadian Society of Plant Physiologists - Edmonton, Canada, 2000

Koch, K.E., Symposium speaker, Molecular Ecophysiology- International Symposium - Darmstadt, Germany

Koch, K.E., Symposium speaker, Banbury Symposium, Cold Spring Harbor, NY,

Koch, K.E., Symposium speaker, CICY research center, Yucatan, Mexico, 2000

Loescher, W.H., Research seminar, Dept of Horticulture and Landscape Architecture , Purdue University, 1999

Long, S.P., Plenary lecture, IUFRO, 2000.

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Long, S.P., Plenary lecture, Brazilian Society of Plant Physiology Annual Meeting, 2001.

Long, S.P., Plenary lecture, ICCDU, Denver, 2001.

Long, S.P., Plenary lecture, International Photosynthesis Congress, Brisbane, 2001.

Long, S.P., Plenary lecture, Western Photosynthesis Conference, Asilomar, 2002.

Markwell, J., Research presentation, Department of Biochemistry, University of Missouri, 2000.

Markwell, J., Plenary Lecture, Society for Experimental Biology, Swansea, Wales, U.K., 2002

Moore, B.D. Research presentation, Department of Plant Biology, Arizona State University, 1999.

Okita, T.W., Symposium speaker, Novartis Foundation Symposium on “Advancing Rice Research With Cutting Edge Science,” International Rice Research Institute, Philippines, 2000.

Okita, T.W., Symposium speaker, Interdisciplinary Plant Physiology and Plant Molecular Biology Mini-Symposium on “Seed Physiology.” Iowa State University, 2001.

Okita, T.W., Symposium speaker, International Symposium (Discovery Meeting) on “Using Model Systems to Accelerate Cereals Research,” CSIRO Plant Industry, Australia, 2001.

Okita, T.W., Symposium speaker, Symposium on “Intracellular Signaling”, 2001 Annual Meeting of the American Society of Plant Biologists, Providence, RI, 2001.

Okita, T.W., Symposium speaker, International Symposium on “Plant Metabolic Engineering," Plant Metabolism Research Center (PMRC), Kyung Hee University, Suwon, Korea, 2001.

Preiss, J., Research seminar, School of Biology, University of Missouri at Kansas City, 2000.

Preiss, J., Research seminar, Max-Planck-Inst. Mol. Plant Physiol. Golm, Germany, 2000.

Preiss, J., Research seminar, Dept. Of Biology, University of Manchester, UK, 2000.

Preiss, J., Research seminar, Center for Molecular Plant Physiology (PlaCe) Plant Biochemistry Laboratory, Department of Plant Biology, KVL, Copenhagen, Denmark, 2001.

Preiss, J., Invited research presentation, 23rd Congress of the Spanish Society of Biochemistry and Molecular Biology, Granada, Spain, 2000.

Preiss, J., Invited research presentation, Øresund Regional Research and Idea Seminar on Starch, Mölle, Sweden, 2001.

Preiss, J., Invited research presentation, American Chemical Society 33RD Great Lakes/Central Regional meeting, Grand Rapids, Michigan, 2001.

Preiss, J. Invited speaker, 27th Meeting of the Federation of European Biochemical Societies in Collaboration with PABMB, Lisbon, Portugal, 2001.

Preiss, J., Invited symposium speaker, X National Congress of Biochemistry and Molecular Biology of Plants; 4th Symposium of Mexico and USA, La Paz, Mexico, 2001.

Portis, A.R., Symposium speaker, Symposium III Redox Regulation. Plant Biology 2000, Annual meeting of the American Society of Plant Physiologists, 2000.

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Portis, A.R., Symposium speaker, Fall Symposium on “Plant Cell Biology and Biochemistry”, Danforth Plant Science Center, St. Louis, Missouri, 2000.

Portis, A.R., Invited research presentation, NIAR/COE/BRIAN-RITE International Symposium on “Photosynthetic CO2-assimilating Enzymes: RuBisCO and PEPC”, Hyogo, Japan, 2000.

Portis, A.R., Symposium speaker, 12th International Congress of Photosynthesis, Brisbane, Australia, 2001.

Randell, D.D., Research presentation, Calgene-Monsanto 2000.

Rodermel, S., Research presentation, University of Iowa, Department of Biology, 1999.

Rodermel, S., Symposium speaker, American Society of Plant Physiologists National Meeting, Baltimore, 1999.

Rodermel, S., Research presentation, UCLA, Department of Chemistry and Biochemistry, 2000.

Rodermel, S., Research presentation, Stanford Univ., Carnegie Institution of Washington 2000.

Rodermel, S., Invited research presentation, NIAR/COE/BRIAN-RITE International Symposium on “Photosynthetic CO2-assimilating Enzymes: RuBisCO and PEPC”, Hyogo, Japan, 2000.

Rodermel, S., Lecturer, FEBS Advanced Course on Chloroplast and Mitochondrial Evolution, Hvar, Croatia, 2001

Rodermel, S., Research presentation, Department of Biology, Johns Hopkins University, 2001

Sassenrath-Cole G.F., Research presentation, Third Annual Geospatial Information in Ag. Conference. Denver CO, 2001.

Sassenrath-Cole G.F., Research presentation, Amer Society Agricul Eng, St. Joseph, MI, 2001.

Spreitzer R.J., Symposium speaker, Minisymposium on Enzymology, American Society of Plant Physiologists annual meeting, San Diego, California, 2000.

Spreitzer R.J., Symposium speaker, VIth International Conference on Carbon Dioxide Utilization, Breckenridge, Colorado, 2001

Spreitzer R.J., Symposium speaker, Xth National Congress of Biochemistry and Molecular Biology of Plants, La Paz, Mexico, 2001.

Spreitzer R.J., Research presentation, Maxygen, Inc, Redwood City, California, 2001

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APPENDIX 4: PROJECT LEADERS

State (Station) Project Leader(s) Areas of Specialization

Florida AES KE Koch Crop Physiology and MolecularBiology

Guam AES TE Marler Plant Physiology

Illinois AES FE Below Crop PhysiologyHJ Bohnert Plant Molecular BiologyS Long Plant Physiology

Illinois ARS AR Portis, Jr. Plant Physiology and Biochemistry

Iowa AES PR Chitnis Plant Biochemistry and MolecularBiology

SR Rodermel Plant Molecular BiologyAD Knapp Plant Physiology

Kansas AES AK Knapp Plant Physiology

Kentucky AES R Houtz Plant Biochemistry and Enzymology

Michigan AES J Preiss Plant BiochemistryW Loescher Plant Physiology and Biochemistry

Minnesota AES R Jones Plant Physiology

Mississippi ARS G Sassenrath-Cole Crop Physiology

Missouri AES DD Randall Plant Biochemistry and Enzymology

Nebraska AES L Allison Plant Molecular BiologyR Chollet Plant Biochemistry and EnzymologyJP Markwell Plant BiochemistryRJ Spreitzer Plant Molecular Biology

Nevada AES J Cushman Plant Biochemistry and Mol Biology

North Carolina AES SC Huber Plant Physiology and Biochemistry(USDA-ARS)

Oregon AES LS Daley Plant Physiology

Pennsylvania AES MJ Guiltinan Plant Physiology

South Carolina AES B Moore Plant Physiology and Biochemistry

Washington AES GE Edwards Plant Biochemistry T Okita Plant Biochemistry

Wisconsin AES SH Duke Plant Physiology and Biochemistry

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APPENDIX 5: AREAS OF PARTICIPATION

ParticipationState (Station) Participant By Objective 1 2 3 4

Florida AES Koch X

Guam AES Marler X

Illinois AES Below XBohnert X XLong X

Illinois ARS Portis X

Iowa AES Chitnis XRodermel X XKnapp X

Kansas AES Knapp X

Kentucky AES Houtz X

Michigan AES Preiss XLoescher X X

Minnesota AES Jones X

Mississippi ARS Sassenrath-Cole X

Missouri AES Randall X

Nebraska AES Allison X XChollet X XMarkwell XSpreitzer X

Nevada AES Cushman X X

North Carolina AES Huber X(USDA-ARS)

Oregon AES Daley X X

Pennsylvania AES Guiltinan X

South Carolina AES Moore X

Washington AES Edwards XOkita X

Wisconsin AES Duke X

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