the biology of melampsora larici-populina pascal frey inra nancy joint research unit « tree –...
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The biology of Melampsora larici-
populina
Pascal FreyINRA NancyJoint Research Unit « Tree – Microbe Interactions »Champenoux, France
Melampsora Genome Consortium - 2008 Summer Workshop
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Poplar rust is caused by several Melampsora spp.
Main disease in commercial poplar cultivation worldwide
Symptoms :
• perturbation of photosynthesis
• early defoliation
• reduction of biomass
High yield losses
• perturbation of automnal translocation
• susceptibility to secondary parasites
Death of young trees
Why sequencing poplar rust ?
© Jean Pinon, INRA Nancy
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• low number of cultivars planted (less than 5 per region)
• monoclonal and even-aged plantations
• large spacing plantations: peeling (veneer, packaging), sawing, particle boards
• Short Rotation Coppice (SRC): biomass and bioenergy
• France is the first poplar wood producer in the EU (ca. 2.5 millions m3/yr)
P. nigra P. trichocarpaP. deltoides
euramerican hybrids
interamerican hybrids
Poplar cultivation in Europe
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A few botanical facts about the genus Populus
Genus Populus :Class : EudicotylédonesClade : Eurosidae IOrder : MalpighialesFamily : Salicaceae (genus Salix and Populus)
Between 29 and >100 species according to different authors.
Eckenwalder’s (1996) classification is widely accepted.Eckenwalder JE (1996) Systematics and evolution of Populus. In Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (Eds), Biology of Populus and its implications for management and conservation, Chap. 1. pp. 7-32. NRC Research Press, Ottawa, Canada.
The genus Populus comprises 6 sections, clustering intercrossing species (also a few cases of inter-sectionnal intercrosses)
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The 6 sections among the genus Populus according to Eckenwalder (1996)
NB: P. maximowiczii = P. suaveolens s.l.
Section Espèce Origine Section Espèce Origine
Aigeiros P. nigra Eurasie P. alba Eurasie
(noirs) P. deltoides Amérique Nord P. tremula Eurasie
P. fremontii Amérique Nord P. tremuloides Amérique Nord
P. trichocarpa Amérique Nord Populus P. grandidentata Amérique Nord
P. balsamifera Amérique Nord (ex-Leuce ) P. guzmanantlensis Mexique
P. angustifolia Amérique Nord P. monticola Mexique
Tacamahaca P. ciliata Himalaya P. sieboldii Asie
(baumiers) P. laurifolia Eurasie P. simaroa Mexique
P. simonii Chine P. gamblei Himalaya
P. suaveolens Asie P. adenopoda Chine
P. szechuanica Chine P. euphratica Eurasie, Afrique
P. yunnanensis Chine Turanga P. ilicifolia Afrique
P. lasiocarpa Chine P. pruinosa Asie
Leucoides P. glauca Asie Abaso P. mexicana Mexique
P. heterophylla Amérique Nord
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P. nigra (N) P. trichocarpa (T)P. deltoides (D)
P. x euramericana (syn. P. x canadensis)
(DxN)e.g. 'Robusta', 'I214'
P. x interamericana (syn. P. x generosa)
(DxT or TxD)e.g. 'Beaupré'
The euramerican and interamerican hybrids
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Rust fungi are excellent botanists !
Aigeiros Tacamahaca Populus
Melampsora spp.P.
nigraP.
deltoidesP.
trichocarpaP.
albaP.
tremulaP.
tremuloides
M. larici-populina + + + - - -
M. allii-populina + + + - - -
M. medusae f. sp. deltoidae + + - - - -
M. occidentalis ? - + - - -
M. pinitorqua - - - + + ?
M. rostrupii - - - + + ?
M. larici-tremulae - - - + + ?
M. magnusiana - - - + + ?
M. pulcherrima - - - + ? ?
M. medusae f. sp. tremuloidae
- - - ? ? +
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The taxonomic position of Melampsora larici-populina
Wingfield et al 2004 Austral. Plant Pathol.
Basidiomycota
Pucciniomycotina
Pucciniomycetes
Pucciniales (= Uredinales)
Melampsoraceae
Melampsora
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larch
poplar
telia andteliospores (n+n)
aecidia (n+n)
plasmogamy
aecidiospores (n+n)
basidiospores (n)
spermogoniaand spermatia (n)
uredinia andurediniospores (n+n)
The life cycle of Melampsora larici-populina: a heteroecious macrocyclic rust
meiosiscaryogamy
basidia (2n)
++
--
X
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++
--
X
sexual reproductionpoplar-larch sympatrymonocyclic3 weeks
asexual reproductionepidemic phase polycyclic5 months
The life cycle of Melampsora larici-populina: a heteroecious macrocyclic rust
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teliaspermogonia
aecia uredinia
basidia
PoplarLarch
© P. Frey, INRA
© P. Frey, INRA
© P. Frey, INRA
© P. Frey, INRA
© P. Frey, INRA
The life cycle of Melampsora larici-populina:
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The life style of Melampsora larici-populina: a strict biotrophic fungus
• M. larici-populina needs fresh plant tissue (poplar leaves) to grow on • Numerous attempts to find artificial culture media for rust fungi, but with limited success (limited mycelial growth, but no infectious spores produced)
• likely due to a very specific interface between the pathogen and the host tissues: the haustorium
© Stéphane Hacquard, INRA
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Matthias Hahn, 2000
The infection process of Mlp: a « lazy » fungus
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The infection process of Mlp: a « lazy » fungus
Laurans & Pilate, 1999, Phytopathology 89: 233-238
2 hrs post inoculation
Rinaldi et al., 2007 Plant Physiol. 144: 347-366
7 days post inoculation
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The Populus-Mlp interaction: a gene-for-gene model
• H.H. Flor 1942: « Each dominant resistance gene in the host plant matches a dominant avirulence gene in the pathogen »
• GFG relationship is very likely in the Populus-Mlp interaction, but not demonstrated yet
• At least 8 qualitative (major) rust resistance genes described in poplar, and 8 avirulence loci in Mlp:
8 virulence loci 28 = 256 possibles pathotypes
Strain 98AG31: Vir3-Vir4-Vir7(Avr1, Avr2, Avr5, Avr6, Avr8)
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Mlp has overcome almost all the R genes released
• Examples:1986: breakdown of R3 ('Luisa-Avanzo')1994: breakdown of R7 ('Beaupré')1997: breakdown of R8 ('Hoogvorst')
• In 2008, of the 130 cultivars available in the UE, only one recently released cv. is completely resistant to Mlp
• Dispersal of Vir7 after the breakdown of R7
1994 1995 1996 1997 1998 1999
(Pinon et al. 1998)
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Mlp has great dispersal capacities
• regional scale: the Durance River valley
• national scale:dispersal of Vir7 in France
• intercontinental scale:Iceland 1999Canada 2002
Wild poplar riparian stands
Poplar-larch sympatry area
annual epidemic annual epidemic
Prelles
St Clément
Rochebrune
Monêtier
Valernes
Les Mées
La Brillanne
Mirabeau
Châteauroux
Embrun
BPR Pont du Fossé
BPR Manse
BPR Manosque
BPR Valernes
BPR Mirabeau
Cultivated poplar stands (R7)
Durance
15 km
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Mlp is among pathogens with highest evolutionnary risk
Linde & McDonald, 2002, Annu. Rev. Phytopathol.
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A nomenclatural issue about Mlp:
Klebahn, 1902. Kulturversuche mit Rostpilzen Z. PflKrankh. PflPath. PflSchutz 12: 43First description of the heteroecious rust fungus M. larici-populina (M. populina = Caeoma laricis)
Saccardo P.A. (1905) Sylloge Fungorum 17: 463 M. laricis-populina
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A nomenclatural issue about Mlp:
• All the literature of the 20th century concerning Mlp used the spelling M. larici-populina
• In 1997, first ITS sequences deposited in GenBank: they use the spelling M. laricis-populina, according to the Index Fungorum
•Taxonomy browser of GenBank :•M. larici-populina : MycoBank (www.mycobank.org)•M. laricis-populina : Index Fungorum (www.indexfungorum.org) and USDA-ARS Systematic Mycology and Microbiology Laboratory, Fungal Databases (http://nt.ars-grin.gov/fungaldatabases)
• DoE JGI portal for Mlp : M. laricis-populina !
• according to some latinists, both can be correct, depending if one considers that larici is an hyphenation of laricis, or that the genetive laricis should apply