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PBIO*3110 – Crop Physiology

Lecture #20

Fall Semester 2008 Lecture Notes for Thursday 13 November

Water Relations II: Stomatal Regulation and the Leaf Energy Balance

How do plants regulate transpiration at the leaf level? What physical processes have the greatest influence in determining leaf temperature?

Learning Objectives

1. Understand how different physical and physiological signals are used by plants to make “decisions” about stomatal regulation of leaf water loss.

2. Know the physical processes that determine leaf temperature in the field, and the relative importance of each one in dissipating the leaf net radiation.

Introduction

In the previous lecture we reviewed the properties of water, and considered the physical processes that determine how water evaporates from leaves, and how water moves through the soil / plant / atmosphere continuum. In the present lecture, we will examine the physiological factors that affect transpiration.

Because soil water is very often the environmental factor most limiting to growth, plants have evolved elaborate physiological mechanisms for regulating their own water use, by altering stomatal conductance. We will see that these mechanisms are extremely dynamic, allowing stomata to open and close in response to a wide variety of environmental factors. Because many

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of these factors fluctuate on the minutes (or even seconds) time scale, stomatal regulation has evolved such that plants can alter stomatal conductance very rapidly.

In addition to its role in determining leaf photosynthetic rates, stomatal conductance is also important with respect to regulating leaf temperature and therefore canopy temperatures. We have already discussed some of the effects of canopy temperatures on crop performance, with respect to photosynthesis, respiration, and plant water relations. In this lecture, we consider how various physical effects determine the canopy temperature. We will see that solar radiation, ambient temperature, wind speed and crop transpiration all have significant effects on the equilibrium temperature of the plant biomass.

The Transpiration ­ Photosynthesis Compromise

When we consider water use efficiency in a future lecture, we will see that crop plants typically transpire on the order of 500 kg of soil water for every kg of new dry matter produced. Since soil water is so often limiting to growth, the question arises: What is the purpose of transpiration? Why do crops use so much water over their growth cycles?

It can be argued that transpiration is essentially a wasteful process, which is a necessary consequence of photosynthesis. That is, crop species would perform better in most environments if their transpiration rates could be minimized, without lowering their photosynthetic rates.

As we have seen, CO2 enters the leaf as a gas through the stomatal pores. The greater the stomatal opening, the less resistance there is to CO2 diffusion into the leaf, and the higher the rate of photosynthesis that can be supported. If the stomatal resistance is too great, the leaf internal CO2 concentration will drop too low, and CO2 will be limiting to photosynthesis. Inside the leaf, CO2 must dissolve in water at the surfaces of mesophyll cells so that it can diffuse across the plasma membrane and eventually to the chloroplast stroma.

Unfortunately, since the cell surfaces inside the leaf must be moist, the interior air spaces of the leaf are almost saturated with water vapour. This water vapour diffuses out the stomata into the drier ambient air. The greater the stomatal opening, the higher the rate of diffusion of water vapour. Thus, transpiration rates tend to vary almost directly with photosynthesis rates. When photosynthesis is occurring rapidly, the stomata are kept relatively open to support high rates of CO2 diffusion into the leaf. This large stomatal opening causes relatively high transpiration rates as well.

Is transpiration entirely a wasteful process? Probably not. In some cases, leaf temperatures are higher than the optimum for photosynthesis (especially in C3 plants, since photorespiration increases at high temperatures). Under these conditions, the evaporation of water from leaves during transpiration can bring about substantial cooling of the leaf tissue, since the latent heat of evaporation must be extracted from the total heat energy of the leaf. This cooling effect can increase the leaf photosynthetic rate, and also protect the leaf from heat­induced injury.

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Schematic representation of the effect of stomatal closure on CO2 uptake and transpiration. Left: gas exchange under normal (water­replete) conditions. Right: gas exchange under drought stress conditions.

Evaporative Demand

Of course, stomatal conductance is not the only factor that determines the transpiration rate. Recall that transpiration is regulated by the law of diffusion (Fick’s law). Therefore, transpiration rates are determined not only by stomatal conductance, but also by the water vapour concentration difference between the interior of the leaf and the ambient air. This difference is commonly termed the vapour pressure differential. Based on our previous considerations of the relationships between air temperature and saturation vapour pressures, we can deduce the following:

• Higher leaf temperatures will lead to greater transpiration rates, since the saturation vapour pressure inside the leaf will be higher.

• Higher ambient relative humidity will tend to decrease transpiration rates, since it increases ambient vapour pressure relative to that of the leaf.

This second point leads to an interesting question: If relative humidity = 100%, does transpiration stop? Can plants photosynthesize without transpiring water under these conditions?

As it turns out, the answer is usually no. Plants will transpire into air at 100% RH, as long as the vapour pressure inside the leaf is greater than that outside the leaf. This is almost always the case, since leaf temperatures are generally higher than air temperatures (since leaves are heated by absorbing solar radiation). Thus, the vapour pressure at 100% RH inside the relatively warm leaf is higher than the vapour pressure at 100% RH in the slightly cooler air.

The term evaporative demand is sometimes used to indicate the dryness of the ambient air. At constant temperature, evaporative demand increases as RH declines. At constant RH, evaporative demand increases as temperature increases. When evaporative demand is high, transpiration will tend to be high, all other factors (leaf temperature, stomatal conductance) being equal.

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Stomatal Regulation

How do plants "decide" on the most appropriate stomatal aperture for any given situation? The physiology of stomatal regulation has been an active area of research for several decades, but there are still many questions that remain unanswered. It is clear that there is more than one control system involved. In fact, stomata seem to sense a variety of environmental parameters and respond accordingly. The precise response depends on the crop species (and perhaps cultivar) as well as the previous history of the plant. Some of the major factors regulating stomatal opening are briefly discussed below.

Factors affecting stomatal opening. Light affects stomatal regulation both directly (blue light perceived by guard cells) and indirectly (PAR increasing photosynthesis and decreasing leaf internal CO2). Although the signal transduction pathway is not fully understood, it is known that these effects cause K+ ions to be actively pumped into guard cells. The resulting decrease in guard cell solute potential causes water to enter the guard cells, thus increasing turgor and causing the stomatal pore to increase in size. A decrease in leaf (or even root) water potential causes the opposite to occur: K+ and water exit guard cells and the stomata close. Abscisic acid (ABA) is known to play a role in inducing stomatal closure under water stress.

Light

Light has both direct and indirect effects on stomata. Blue light (especially) can bring about stomatal opening directly. The mechanisms by which the light is perceived, and the subsequent signal transduction pathway, are currently under investigation. Light can also indirectly cause stomatal opening via photosynthesis, by decreasing the leaf internal CO2 concentration (see below).

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CO2

Stomata open as leaf internal CO2 declines, in order to reduce the resistance to CO2 diffusion into the leaf. Thus, as photosynthesis increases (for instance, in response to an increase in PPFD), stomata open. If photosynthesis decreases, leaf internal CO2 increases, and stomata close. C4 grasses such as corn are very sensitive to leaf internal CO2, and stomata open and close rapidly in response to natural fluctuations in PPFD and photosynthesis. Drastically increasing [CO2] in the air around a leaf will usually cause at least transient stomatal closure.

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Changes in photosynthesis (AN), stomatal conductance (g) and leaf internal CO2 concentration (ci) of a corn leaf in response to fluctuations in incident PPFD. (Data of H.J. Earl)

Leaf Water Status

As leaf water potential drops, stomata tend to close. Again, this effect may be direct or indirect. If water potential is very low, the guard cells themselves, and the surrounding subsidiary cells, may lose turgor, causing stomatal closure directly.

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Much more often, the response to leaf water potential is indirect. As leaf water potential drops, the content of ABA in the leaves increases. This ABA appears to sensitize the stomata to other signals that would normally cause closing, and so the average stomatal aperture is decreased.

Soil Water Potential

Obviously, as soil water content drops, leaf water potential also declines (and xylem tension increases). Thus, low soil water potentials indirectly causes stomatal closure by causing a decrease in leaf water potential. However, it is now well established that low soil water content can lead to stomatal closing even in the absence of a change in leaf water potential.

It appears that as the soil dries, the roots "sense" the lower soil water potential, and synthesize ABA. This ABA is transported to the leaves in the transpiration stream (i.e., via the xylem), and produces the same effect on stomata as leaf­source ABA. This mechanism may allow plants to anticipate drought conditions and respond accordingly, even before the leaf water potential has been affected.

Some species also open stomata in response to extremely high soil water content. This can occur even at night, and presumably has the advantage of depleting soil water and thus preventing root anaerobiosis.

Temperature

Leaf temperatures may indirectly affect stomatal opening in several ways. For instance, changes in temperature affect the photosynthetic rate, and therefore alter leaf internal CO2 ­ stomata respond on the minutes time scale to such changes in CO2, as we have seen above. Also, high temperatures cause leaf internal vapor pressure and therefore transpiration to increase. This may lead to a reduction in leaf water potential, causing stomata to close.

Temperature may also have a more direct effect on stomata. In most species, deleteriously high leaf temperatures may induce stomatal opening, even when leaf internal CO2 is not limiting to photosynthesis. (The effect occurs even in darkness.) This appears to be a strategy designed to decrease leaf temperatures through evaporative cooling.

Daily Patterns of Stomatal Activity

Some typical daily patterns of stomatal opening and closing are shown in the figure below. In general, stomatal opening tends to follow the incident PPFD over the day, being less on cloudy than on clear days.

The effect of a dry soil is also shown; in the morning, stomatal apertures are relatively high, but much of the transpiration is occurring at the expense of water stored in plant tissues. As this is depleted, leaf water potential declines and stomatal closing ensues.

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Even in moist soils, resistance to water movement through the plant may result in low leaf water potentials and stomatal closing around solar noon; this can produce the "W­function" stomatal pattern.

Response of stomata to environmental conditions (top), and typical daily patterns of stomatal opening. (From Salisbury and Ross, 1992)

The Leaf Energy Balance

The law of energy conservation (a.k.a. The First Law of Thermodynamics) states that energy can neither be created nor destroyed, but that it may be converted from one form to another. Leaves in a crop canopy that are illuminated by sunlight absorb energy primarily as shortwave and long­ wave radiation. They dissipate this energy in different forms, through a number of physical processes, including:

• emittance of long­wave radiation • convection (movement of warm air away from leaves) • evaporation of water (transpiration) • conduction (warming of their surroundings by direct contact)

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• storage of energy, either as heat energy in tissues, or chemical potential energy in the products of photosynthesis.

We will now consider the nature of each of these processes, and their relative magnitudes under realistic conditions.

Net Radiation

Recall that every object radiates energy in the electromagnetic spectrum, and that the wavelengths radiated, as well as the total energy radiated, are dependent on the object's temperature. Leaves receive short­wave radiation from the sun, both as direct and diffuse (reflected) radiation, as well as long­wave radiation from objects in their surroundings. In turn, leaves also radiate energy in the long­wave band.

Leaves absorb energy in both the short­wave and long wave regions of the electromagnetic spectrum, and radiate energy in the long­wave region. The amount of energy radiated from leaves can be easily calculated if the leaf temperature is known.

A sunlit leaf in a crop canopy might be exposed to 1000 W m ­2 total short­wave radiation. However, not all of this is actually absorbed by the leaf. As we have seen previously, radiation in the PAR region is absorbed very efficiently by leaves (approximately 89%). However, other parts of the short­wave band (UV, IR) are very poorly absorbed. As a result, average leaf absorptance of total sunlight is only about 50%.

By contrast, long­wave radiation is very efficiently absorbed by leaves (about 96%). Let us consider an example leaf that receives a total of 1000 W m ­2 short­wave radiation and 800 W m ­2 long­wave radiation (total for both sides of the leaf). The total energy absorbed by the leaf (QT) is then:

QT = 0.50 × 1000 W m ­2 + 0.96 × 800 W m ­2 =

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= 500 W m ­2 + 768 W m ­2 =

= 1268 W m ­2 .

This is a substantial amount of energy. However, a large portion of this is re­radiated from the leaf as long­wave radiation. Recall the equation that predicts the amount of long­wave energy radiated per unit surface area of an object such as a leaf (QR, in W m ­2 )[see Lecture #5]:

QR = ε × σ × T 4 ,

where, ε is the longwave emissivity of the object σ is the Stefan­Boltzmann constant (5.673 x 10 ­8 W m ­2 K ­4 ) T is the temperature of the object, in K.

Long­wave emissivity is the same as absorptance (i.e., 0.96 for leaves). Thus, if we assume that our example leaf has a temperature of 30°C (303 K), we can calculate the quantity of long­wave radiation emitted:

QR = 2 × 0.96 × (5.673 × 10 ­8 W m ­2 K ­4 ) × (303 K) 4 =

= 918 W m ­2

(Note the factor of 2 introduced at the beginning of the equation. This is to account for the fact that the leaf radiates from both its upper and lower surfaces.)

Net radiation received by the leaf (QN) may now be calculated as the difference between QT and QR. In our example, QN is equal to 350 W m ­2 (i.e., 1268 ­ 918). If this energy were not somehow dissipated, the leaf would increase in temperature very rapidly. Below, we examine in detail the physical processes that allow leaves to dissipate the energy represented by QN.

Energy Dissipation

As mentioned above, besides emitting longwave radiation, leaves may dissipate energy through a number of physical and chemical processes. These are represented schematically in the figure below. Let's continue with our example, and calculate the relative magnitude of each of these processes with respect to the dissipation of our 350 W m ­2 of net radiation.

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Five physical / chemical processes by which leaves may dissipate energy.

1. Metabolism

The energy stored as chemical potential energy in the products of photosynthesis can be subtracted from the total energy balance of the leaf. However, a simple calculation shows that this energy is not a significant fraction of the net radiation calculated above.

Consider a leaf with a high net photosynthetic rate, say AN = 20 µmol CO2 m ­2 s ­1 . This equates to a rate of glucose production of 0.60 mg glucose m ­2 s ­1 (can you show this?) The energy content of one mg of glucose is 16 J. Therefore, the rate of energy storage as glucose is:

(0.60 mg glucose m ­2 s ­1 ) (16 J mg ­1 glucose) = 9.6 J m ­2 s ­1 = 9.6 W m ­2 .

This amounts to a mere 2.7% of our QN value of 350 W m ­

2. Storage

Heat energy may be simply stored by the canopy, if the temperature of the biomass is increasing. However, this can also be shown to be a minor portion of the total energy balance.

Imagine that our example leaf has a fresh weight of 300 g m ­2 . For the sake of simplicity, assume that the leaf is composed entirely of water (rather than being only about 90% water). The specific heat capacity of water is 4.182 J g ­1 K ­1 . Thus, if the temperature of the leaf is increasing by 5 K (or 5 °C) per hour, then the energy stored in the tissue would be:

(300 g m ­2 ) × (4.182 J g ­1 K ­1 ) × (5 K h ­1 ) / (3600 s h ­1 ) = 1.74 J m ­2 s ­1

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Obviously, energy storage by the leaf can not account for a significant percentage of QN in our example.

3. Conductance

Heat may be dissipated via conductance. That is, direct contact between the plant tissue and some other object, such as the soil, may allow heat energy to be transferred from the warmer object to the cooler one.

Estimating conductance is difficult from a computational standpoint. However, for individual sunlit leaves, conductance represents a very minor portion of the total energy balance, and can therefore be safely ignored.

4. Transpiration

Evaporation of water in the interior of the leaf results in cooling due to the latent heat of vaporization required to allow the water to enter the gas phase. Since we have already considered the equations required to calculate the transpiration rate, it is a simple matter to then multiply the rate of transpiration by the molar latent heat of vaporization (λ, 43 200 J mol ­1 ) to determine the energy dissipated by this process. For our example assume the following:

leaf temperature = 30°C air temperature = 25°C relative humidity = 75% total conductance to water vapor (gw) = 0.25 mol m ­2 s ­1 ambient pressure = 100 kPa

With this information, we can calculate the vapour pressure inside the leaf as 4.26 kPa, and the vapor concentration is therefore 0.0426 mol mol ­1 . Similarly, the vapour concentration outside the leaf is determined to be 0.0239 mol mol ­1 (be sure that you can calculate these.) The transpiration rate is therefore:

E = (wi ­ wa) gw =

= (0.0426 ­ 0.0239) × (0.25 mol m ­2 s ­1 ) = 4.68 x 10 ­3 mol m ­2 s ­1

To calculate the energy dissipated via the evaporation of water, we simply multiple the transpiration rate by λ:

λE = (4.68 x 10 ­3 mol m ­2 s ­1 ) × (43 200 J mol ­1 ) = 202 J m ­2 s ­1

In our example, the latent heat of evaporation associated with transpiration accounts for 57% of QN.

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5. Convection

The other major process by which leaves can dissipate heat energy is the process of convection. Because the leaf is warmer than the surrounding air, heat is transferred from the leaf to the air. This warmer air is moved away from the leaf due to normal turbulence, and the leaf experiences a net loss of heat.

The rate at which convection removes heat from the leaf depends on (a) the temperature difference between the leaf and the air and (b) the conductance to movement of warm air away from the leaf (gA). This is directly analogous to the process of diffusion:

convective heat loss = (leaf temp. ­ air temp.) × gA × 29.2 J mol ­1 °C ­1 ,

where 29.2 J mol ­1 °C ­1 is the (approximate) molar heat capacity of air

Note that gA is a function of both windspeed and physical properties of the leaf itself that affect air turbulence near the leaf surface (a thick "boundary layer" of unstirred air next to the leaf tends to decrease gA).

In our example, let us assume a value of 0.93 mol m ­2 s ­1 for gA. Convective heat loss is then:

C = (30°C ­ 25°C) × (0.93 mol m ­2 s ­1 ) × (29.2 J mol ­1 °C ­1 ) =

= 136 J s ­1 m ­2 = 136 W m ­2

This is equivalent to 39% of QN in our example.

Summary

In our example, 500 W m ­2 were absorbed by the leaf as short­wave (solar) radiation, and an additional 768 W m ­2 were absorbed as long­wave radiation, for a total of 1268 W m ­2 . Of this, 918 W m ­2 were re­emitted as long­wave radiation, leaving a net radiation (QN) of 350 W m ­2 .

The major routes of dissipating this QN were evapotranspiration (57%) and convection (39%). Small amounts of dissipation may also be attributed to photosynthesis (chemical storage of energy), warming of the canopy (physical storage of energy) and conductance of heat from the vegetation to the soil.

Finally, it should be noted that the proportions attributable to each of these dissipative processes change markedly with environmental ­ physiological conditions. For example, closure of stomata in our example would cause leaf temperature to rise, due to a decrease in evaporative cooling. However, the magnitude of this increase in leaf temperature would then be moderated by changes in the other two major routes for energy loss (long­wave radiation and convective heat loss), both of which increase with leaf temperature.