Open access peer-reviewed chapter

The physiology and genetics of stomatal adjustment under fluctuating and stressed environments

Written By

Mingnan Qu, Saber Hamdani and James A. Bunce

Submitted: September 9th, 2015 Reviewed: January 11th, 2016 Published: March 30th, 2016

DOI: 10.5772/62223

Chapter metrics overview

1,995 Chapter Downloads

View Full Metrics


Stomata are pores in the leaf that allow gas exchange where water vapor leaves the plant and carbon dioxide enters. Under natural condition, plants always experience at a fluctuating light regime (shade-/sun-fleck) and due to global climate change, occasionally extreme high temperature and CO2 enrichment will be inevitable occurred, which dramatically affects stomatal response, and trade-off between water-use efficiency and photosynthesis. Response of stomata to fluctuating and stressed environments determines optimized strategy of plants directing to water save or photosynthesis. Dynamic adjustments of stomata play an equivalent role as steady-state stomatal characteristics. Evolutionary approach indicated that stomatal-dynamic adjustments interacting with historical environments or life histories could be genetically controlled and environmentally selected. In this article, we reviewed physiological response of stomatal dynamic to changing enironments including our previous works, and discussed the possibility of genetic improvements on stomatal adjustments by estimating broad-sense heritability and SNP heritability of stomatal pattern. To gain insight into the framework of stomatal genetics, we highlighted the importance of combining multidisciplinary techniques, such as mathematic modeling, quantitative genetics, molecular biology and equipments developments.


  • Stomatal dynamics
  • Changing environments
  • Photosynthesis
  • Evolution

1. Introduction

Stomata, from the Greek word “stoma” meaning mouth, are small pores that distributed on the epidermis of plant leaves. Their structures consist of two guard cells around a pore. For optimum efficiency, stomata must balance the gas exchange between inside and outside the leaf, in order to maximize CO2 uptake for photosynthetic carbon assimilation (PN) and to minimize water loss through transpiration (E). Although the cumulative area of stomatal pores only represents a small fraction of the leaf surface, typically less than 3%, the CO2 uptake and water loss pass through these pores. When fully open, they can promote water evaporation equivalent to one-half of a wet surface of the same area [1]. To cope with environmental stress during growth condition, plants must adjust and regulate the stomatal opening/closing process to obtain optimized transpiration and leaf water status.

On the other hand, studying the evolutionary adaptation and natural variation of stomata-related genes may represent an essential step for better understanding the mechanisms involved in the stomatal adjustment and regulation. In fact, stomata have probably undergone a crucial adaptation occurring 400 million years ago, it enabled plants to thrive on land. To survive in the dry atmosphere, plants must maintain a reasonable level of gas exchange necessary for PN and E, in order to protect against desiccation [2]. In addition, the natural variation in stomata-related genes across different cultivars (from different origins) of particular species may indicate differing selection pressures allowing better adaptation against environmental stress [3].

To get a deeper understanding, the study of the relationship between genotype and phenotype at the organism–environment interface by identifying traits that respond to differing environmental pressures and uncovering the genetic basis for variability in these traits is highly requested. Recent researches have shown that the mode of action of stomatal movement depends on the combination of environmental and intracellular signals. These external factors (e.g., CO2, biotic and abiotic stresses, and additionally different plant hormones) and internal signals (e.g., ion exchange, metabolites, catalyze of enzyme, and gene structure or expression) simultaneously affect stomatal dynamics, forming a complex framework behind acclimation responses of plants under fluctuating and stressed environments. The empirical evidences related to stomatal dynamics provide strong promotion for the development of model stimulating stomatal dynamics, which remains difficult to achieve so far. In this chapter, we aim to give a multidimensional review about recent works describing multiple environmental and internal factors, such as elevated CO2, heat stress, light fluctuations, ion channel, and stomata-related genes [48]. Furthermore, we discussed expended research perspective regarding stomatal evolution, natural variations of stomatal traits, interactions with life history, and theoretical modeling.


2. External environments

2.1. Interactive effects of elevated CO2 and heat wave

The global change, leading to frequent occurrence of atmospheric CO2 enrichment and heat wave, inevitably affects the development and final productivity of plants. Most climate impact studies rely on changes in means of meteorological variables, such as temperature and rainfall, to estimate the potential climate impacts on agricultural production. However, extreme meteorological events, e.g., a short period of abnormally high temperatures, can have a significant profound and lasting effect on canopy transpiration, crop growth, and final yield [9].

During heat stress, elevated CO2 has probably less effect on C3 plants as compared to C4 plants [10]. In fact, elevated CO2 can increase water-use efficiency (WUE) by decreasing stomatal conductance (gs) and E[11], which may increase tolerance to acute heat. It was shown that the reduction in gs (stomatal opening) is about 20% for C3 and 50% for C4 species [10, 12, 13]. The lower gs in C4 plants may induce lower transpiration (water loss) and thus higher leaf temperatures, which may increase heat-related damage in C4 plants as compared to C3 plants in the same habitat.

Since evaporative cooling is essential to avoid heat damage in leaves exposed to full sunlight, and time scales of stomatal adjustments are longer than fluctuations in solar irradiance within a canopy, the question arises whether elevated CO2 can mitigate damage over transpiring leaves from extreme high temperature by decreasing gs. If this is the case, then adaptation for cooling would appear as a more imperative driver for stomatal adjustments than the potential increase in carbon gain. To test this hypothesis, intact leaves of maize were subjected to a substantial reduction PN due to 45°C heat stress cycle for 1hour[14]. Our previous finding showed that elevated CO2, either during plant growth or co-heat period, does not improve the foliar thermotolerance against heat stress (Figure 1). With the lower PN and higher gs and subcellular CO2 pressure (Ci) following the acute heat stress treatment, a non-stomatal inhibition of gs occurs, contrary to other studies showing a stomatal adjustments in response to high temperature stress in grape leaves [15, 16]. In the meantime, the sudden reversal of stomatal responses to leaf temperature and CO2 between 40°C and 45°C (Figure 1) suggests that to avoid damage, plants enhance the stomatal opening, leading to an increase in evaporative cooling.

Some studies compared elevated CO2 effects with tolerance to heat stress in relatively heat-sensitive vs. heat-tolerant species or in species with different photosynthetic pathways [4, 1720]. As an example, two corn cultivars (B73 and B106) were previously reported as contrasting heat stress tolerance from field investigation and evaluations [21]. When comparing the effects of elevated CO2 and heat stress from field-based investigation using these corn cultivars, our previous results showed a reversible response of two cultivars regarding to photosynthetic activity (Figure 2), which might be due to intricate reasons: 1) change in physical function of stomatal regulation by decreasing transpiration and optimized water conservation at intact leaves scales; 2) change in kinetic activities of photosynthetic regulatory enzymes, i.e., rubisco (ribulose 1,5-bisphosphate carboxylase/oxygenase), PEPase, and MDHase (Table 1), which agrees with some reports [22, 23]; and 3) disorder of metabolite flux in Calvin cycle due to heat stress.

2.2 Fluctuating light effects

Leaves are always subjected to rapidly fluctuating irradiance due to motion of sunflecks and clouds that may span two orders of magnitude from light compensation points of shade-adapted leaves to almost full irradiance intensities [25]. Such environmental fluctuations occur at second scales, which is much shorter than the time needed for stomatal adjustments (2–60 min.) [26]. For leaves with slowly adjusting stomata, rapid fluctuations at shorter time scales could push leaf hydraulic and thermal status beyond operational limits resulting in xylem cavitation, overheating, or wilting.

Figure 1.

Dynamic changes of photosynthetic parameters during acute heat stress cycles. Lines with same color stand for treatment at same exposure CO2 concentrations. Symbols GambEamb, GambEelv, GelvEamb, and GelvEelv represent grown and exposed at ambient [CO2], grown at ambient [CO2] but exposed at elevated [CO2], grown at elevated [CO2] but exposed at ambient [CO2], and both of grown and exposed at elevated [CO2].Vertical barsrepresent S.E. forn= 9 (see [14]).

Figure 2.

Heat induced decrease of photosynthesis and stomatal conductances in B76 and B106. Black and grid bars represent ambient and elevated [CO2], respectively. Ratio of photosynthesis and stomatal conductances under heat stress over control in B76 and B106 was shown in inserted panel. (Qu et al. 2016, unpublished data).

Although the phenomena underlying dynamic responses of photosynthesis to sunflecks (such as induction requirements) were studied by physiologists and biochemists earlier [26], their role in sunfleck utilization was not recognized until the early 1980s. Evidence for the light activation requirement of the primary carboxylating enzyme, Rubisco, was first uncovered in the 1960s [27]. The components underlying induction, especially stomatal behavior, are complex and are dependent on environmental and developmental factors as well transient light changes. It was reported that water stress could reduce gs in shade-grown, but not in sun-grown for the leaves of a Populusspecies; drought also could lead to faster induction gain in shade-grown, but not in sun-grown for the leaves during simulated sunflecks [28] .

OTCsHeatPEPC activity
(μmol m−2 s−1)
ME activity
(μmol m−2 s−1)
MDH activity
(μmol m−2 s−1)
B76aft015.5 ± 0.5
(33.1 ± 1.6)
3.7 ± 0.4
(31.6 ± 0.5)
7.9 ± 3.4
(24.8 ± 3.3)
aft419.7 ± 0.5
(36.5 ± 1.5)
20.6 ± 0.3
(29.0 ± 0.1)
14.9 ± 1.2
(26.5 ± 0.4)
% Change27.1456.888.6
B106aft013.3 ± 0.7
(32.8 ± 0.5)
12.4 ± 1.1
(24.6 ± 0.3)
17.2 ± 0.3
(26.1 ± 0.2)
aft415.8 ± 0.7
(36.6 ± 1.4)
13.9 ± 0.7
(27.7 ± 0.3)
19.0 ± 2.7
(28.9 ± 0.4)
% Change18.812.110.5
B76aft013.6 ± 1.5
(32.0 ± 0.7)
10.9 ± 0.2
(25.3 ± 0.4)
12.1 ± 1.7
(29.0 ± 1.2)
aft417.9 ± 1.3
(34.4 ± 0.9)
18.1 ± 1.0
(26.3 ± 0.6)
20.9 ± 0.4
(28.8 ± 1.5)
% Change31.666.572.7
B106aft010.5 ± 1.7
(32.2 ± 0.1)
9.0 ± 0.6
(26.7 ± 0.8)
14.6 ± 1.7
(28.6 ± 0.6)
aft412.8 ± 1.0
(31.9 ± 1.0)
11.6 ± 1.6
(29.2 ± 0.5)
13.7 ± 0.9
(31.6 ± 1.1)
% Change21.929.1-6.2

Table 1.

Enzyme activities of PEPC, NADP-ME, and NADP-MDH for B76 vs. B106 grown ambient and elevated [CO2]. Values of control experiments were shown in brackets (Qu et al. 2016, unpublished data).

In the naturally fluctuating environment, the temporal disconnect between gs and PN means the coordination between carbon gain and water loss (and, therefore, WUE) is far from optimal ([29]; Figure 3). Photosynthetic induction state is a complex function of light-dependent stomatal opening and closing responses and the time courses of light-regulated enzyme activation and deactivation. All these combined factors determine the potential light-saturated PN at any given time and therefore the potential PN that can be achieved during a fluctuating light (shade-fleck). Under this condition, responses of gs and PN are not always synchronized, as stomatal movements can be an order of magnitude slower than the more rapid photosynthetic response to the same environmental stimuli ([30, 31]; Figure 3).

Figure 3.

Photosynthesis and stomatal conductance in response to naturally light regime (Qu et al. 2016, unpublished data).


3. Internal signals

3.1 Ion channels and transmembrane antiporters

There is no question that stomatal movements (stomatal opening and closing) of seed plants, including crop plants, arise from the transport, accumulation, and release of osmotically active solutes (reviewed by [32]). It has been shown that the guard cell movement is controlled by movement of Cl+, Na+, K+, and also changes in the sucrose and malate levels [32, 33]. It is reasonable to give expectation that ion exchange, inducing change in pH, might indirectly determine response time of stomatal adjustments during light fluctuations based on previous literatures. For example, membrane depolarization in ABA stimulates K+ efflux within seconds through outward-rectifying K+ channels, in Arabidopsis the GORK K+ channel [34, 35], and these K+ currents are enhanced during the subsequent 3–5 min as a consequence of rise in cytosolic pH [36, 37]. Stomatal aperture responds more slowly, typically with half-times of 10–20 min, reaching a new stable, (near) closed state after 45–60 min [3840]. Thus, making a connection of ion channel antiporters to the speed and efficacy of stomatal movements is necessarily important.

3.2 Anatomical features of stomata

Responsiveness of stomatal adjustments under changing environments is also dependent on anatomical characteristics. In fact, stomatal anatomical features define the maximum theoretical conductance and also influence the speed of response [41]. Many experimental evidences have demonstrated that stomatal density is negatively correlated with stomatal size [42, 43]. The interaction/correlation between stomatal size and density and the impact on stomatal function have received much attention [44]. The latest studies have also implied that physical attributes affect stomatal response times following environmental perturbations [45]. Therefore, it is possible to manipulate the stomatal structure, for example, we can take into consideration the interaction between stomatal size and number and its impact on rapidity of stomatal movement.

3.3 Casual genes of stomatal features

Engineering and breeding crops for enhanced drought resistance become a pressing task for plant biologists and breeders. Manipulation on functional genes underlying dynamics of stomatal responses and steady-state values of gs would be helpful for optimizing WUE and drought resistance of plants [4651]. For example, mutation in the SLAC1gene, which codes for an anion channel, causes slow stomatal opening by light, low CO2, and elevated air humidity in intact plants, due to severely reduced activity of inward K+ channels in slac1guard cells [52]. Arabidopsis (Arabidopsis thaliana) stomatal density and distribution (sdd1-1) mutants, having a point mutation in a single gene that encodes a subtilisin-like Ser protease, exhibit a 2.5-fold higher stomatal density compared with their wild type [53]. Stomatal movements can also be stimulated by membrane fusion protein, soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor (SYP121), Eisenach et al. [54] demonstrated that stomatal opening and the rise in stomatal transpiration of the syp121mutant were delayed in the dark–light transition and following the Ca2+-evoked closure. The increase in stomatal density translates leads to an increase in gs and 30% greater PN under high light conditions [55]. Tanaka et al. [56] have used plants overexpressing STOMAGEN, a positive regulator of stomatal density, to produce transgenic plants with a two- to three fold greater stomatal density than the wild type. PN in these plants is increased by 30% due to greater CO2 diffusion into the leaf rather than changes in photosynthetic carboxylation capacity [56]. By contrast, some genes can induce low stomatal density and gs at high light intensities, for example, upregulation of sdd1can restrict CO2 diffusion limited PN to 80% of the wild type [57].

These findings exemplify the role of both the physical and functional stomatal features in determining gs. In particular, these works illustrate the importance of surrounding environmental conditions and ion exchange on stomatal behavior and the significance of examining gs limitation on PN at fluctuating light and elevated CO2 and heat stress.


4. Natural variation and heritability of stomatal conductance

The analysis of evolution of stomata over species should depend on two strategies, i.e., fossil studies on ancestor plants and genetic studies on current plants. Fossil evidence shows that stomata have occurred in sporophytes and (briefly) gametophytes of embryophytes during the last 400 million years. Cladistic analyses with hornworts basal are consistent with a unique origin of stomata, although cladograms with hornworts as the deepest branching embryophytes require loss of stomata early in the evolution of liverworts (reviewed by [58]).

Genetic variation is a vital characteristic of every population that is required to adapt. Phenotypic trait variance within a population can be related to genetic variance as an estimation of broad-sense heritability (H2). In theory, when a greater proportion of phenotypic variation is attributable to genetic variance, the corresponded trait is highly heritable. Exploring stomatal traits with high H2 under multiple environments could provide strategy for artificial selection and improvements on stomatal traits. Although natural variation in photosynthetic capacity especially stomatal features is known to exist among different species [5963], relatively few studies have examined natural variation among accessions of the same species [6467]. Besides, studying the genetic variation of photosynthetic capacity of different rice accessions with diverse genetic background could be an effective way to improve the photosynthetic capacity of existing rice elite germplasm [67, 68].

In fact, mining natural variations of photosynthetic and stomatal parameters is regarded as a promising approach to identify new genes or alleles for crop improvement. Conventionally, the identification of genomic loci that govern complex traits has been extensively facilitated by the development of quantitative trait locus (QTL) mapping approaches. Recent advances in high-throughput and high-dimensional genotyping and phenotyping technologies enable us to reduce the gaps between genomics and phenomics using the principles of genome-wide association studies (GWAS). This biostatistic method has been widely used in food crops for identifying genes that underlie natural variation of various ecological and agricultural traits [6971]. Consequently, a combination of GWAS and QTL mapping as well as co-expression network would be a better option to obtain additive, dominance, and epistasis effects of genes, for example, in Arabidopsis [72] and soybean [73].

Therefore, understanding the mechanisms that underlie efficient carbon gain driven by stomatal adjustments in fluctuating light can open doors for increasing plant yields and, more broadly, can reveal fundamental principles to optimize the water cycle system in the biosphere.


5. Relation of stomatal profiling with life histories

Evolutionary responses of stomata to fluctuating light conditions are important because stomata in theory must have been subject to evolutionary pressures associated with highly variable conditions. This is always related to the life history of accession origins. Studying the evolution of photosynthesis is critical to understand how stomata or plants structure variation influence ecological interactions and adaptation to various environments [74]. Where an overlying geographical origin or environmental gradient exerts strong adaptive selection, the natural variation in both genotype and phenotype is predicted. However, this variation will depend on the relative strength of selection, demographic history, and levels of dispersal and/or gene flow among populations [75]. Differing selection pressures may include temperature, precipitation, and soil nutrient availability, growing season length, photoperiod, and biotic agents. Many of these factors are directly affected by geographic conditions and are therefore interrelated. This is already extensively reported in trees species. Genetic covariance among ecophysiological traits can be shaped by the past ecological and evolutionary processes [3]. However, for traits of ecological or evolutionary interest, studies must also address the extent to which population structure, trait variation, and genetic architecture covary along ecological gradients [3].


6. Theoretical modeling for describing stomatal delays

To describe the dynamics of gs and PN in response to an abrupt change in light, piecewise linear, logistic, and exponential models have been frequently employed [25, 7678]. For instance, in terms of stomatal dynamics in time scales during closing (τcl) and opening phases (τop), significant variation insensitivity and responsiveness is known to exist among different species [25, 32, 33]. As described above, when switching from high to low light, stomata always performed a lag relative to photosynthetic reduction, and to simplify, linearizing imputation between specific time period (stepwise) on photosynthetic dynamics could be a better option to define the amplitude and speed of stomata. In Arabidopsis, Wang et al. [79] have developed a dynamic model of stomatal responses, taking into consideration ion channel and kinetic effects as components controlling gs under steady-state and dynamic conditions. This model integrated the biophysical, molecular, and biochemical characteristics of guard cell transport, malate metabolism, and H+ and Ca2+, to predict stomatal aperture, which can be used to explore inherent interaction between different factors controlling gs [79, 80]. This model provided a good framework to incorporate new knowledge about controls over guard cell movements and hence help design engineering options to gain optimal steady state gs and also optimal dynamic responses of gs to light levels.


  1. 1. Willmer C, Fricker M. 1996. Stomata, 2nd edn. London: Chapman & Hall.
  2. 2. Petersona KM, Rychela AL, Toriia KU. Out of the mouths of plants: The molecular basis of the evolution and diversity of stomatal development.The Plant Cell22: 296–306.
  3. 3. McKown AD, Guy RD, Klateps J, Geraldes A, Friedmann M, Cronk QCB, El-Kassa YA, Mansfield SD, Douglas CJ. 2014a. Geographical and environmental gradients shape phenotypic trait variation and genetic structure inPopulus trichocarpa. The New Phytologist 201: 1263–1276.
  4. 4. Taub , DR, Seemann JR, Coleman JS. 2000. Growth in elevated CO2 protects photosynthesis against high-temperature damage.Plant, Cell & Environment23: 649–656.
  5. 5. Wang D, Heckathorn SA, Barua D, Joshi P, Hamilton EW, LaCroix JJ. 2008. Effects of elevated CO2 on the tolerance of photosynthesis to acute heat stress in C3, C4, and CAM species.American Journal of Botany95: 165–176.
  6. 6. Wang D, Heckathorn SA, Hamiton EW, Frantz J. 2014. Effects of CO2 on the tolerance of photosynthesis to heat stress can be affected by photosynthetic pathway and nitrogen.American Journal of Botany101: 34–44.
  7. 7. Yang Y, Han C, Liu Q, Lin B, Wang J. 2008. Effect of drought and low light on growth and enzymatic antioxidant system ofPicea asperataseedlings.Acta Physiologiae Plantarum30: 433–440.
  8. 8. Demmig B, Winter K, Kruger A, Czygan FC. 1988. Zeaxanthin and the heat dissipation of excess light energy inNerium oleanderexposed to a combination of high light and water stress.Plant Physiology 87: 17–24.
  9. 9. Mearns LO, Katz RW, Schneider SH. 1984. Extreme high temperature events: changes in their probabilities with changes in mean temperature.Journal of Climate and Applied Meteorology23: 1601–1613.
  10. 10. Sage RF. 1994. Acclimation of photosynthesis to increasing atmospheric CO2: The gas-exchange perspective.Photosynthesis Research39: 351–368.
  11. 11. Ainsworth EA, Davey PA, Bernacchi CJ, Dermody OC, Heaton EA, Moore DJ, Morgan PB, Naidu SL, Ra HSY, Zhu XG, Gurtis PS, Long SP. 2002. A meta-analysis of elevated CO2 effects on soybean (Glycine max) physiology, growth and yield.Global Change Biology8: 695–709.
  12. 12. Reich PB, Tilman D, Craine J, Ellsworth D, Tjoelker MG, Knops J, Wedin D, Naeem S, Bahauddin D, Goth J, Bengtson W, Lee TD. 2001. Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? A field test with 16 grassland species.The New Phytologist150: 435–448.
  13. 13. Maherali H, Reid CD, Polley HW, Johnson HB, Jackson RB. 2002. Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland.Plant, Cell & Environment25: 557–566.
  14. 14. Qu M, Bunce JA, Shi ZS. 2014. Does elevated CO2 protect photosynthesis from damage by high temperature via modifying leaf water status in maize seedlings?Photosynthetica52: 211–216.
  15. 15. Luo HB, Ma L, Xi HF, Duan W, Li SH, Loescher W, Wang JF, Wang LJ. 2011. Photosynthetic responses to heat treatments at different temperatures and following recovery in grapevine (Vitis amurensisL.) leaves.PLoS ONE6: e23033. doi:10.1371/journal.pone.0023033.
  16. 16. Hamilton EW, Heckathorn SA, Joshi P, Wang D, Barua D. 2008. Interactive effects of elevated CO2 and growth temperature on the tolerance of photosynthesis to acute heat stress in C3 and C4 species.Journal of Integrative Plant Biology50: 1375–1387.
  17. 17. Coleman JS, Rochefort L, Bazzaz , Woodward . 1991. Atmospheric CO2, plant nitrogen status and the susceptibility of plants to acute heat stress.Plant, Cell & Environment14: 667–674.
  18. 18. Bassow SL, McConnaughay KDM, Bazzaz FA. 1994. The response of temperate tree seedlings grown in elevated CO2 to extreme temperature events.Ecological Applications4: 593–603.
  19. 19. Roden JS, Ball MC. 1996. Growth and photosynthesis of two eucalypt species during high temperature stress under ambient and elevated [CO2].Global Change Biology2: 115–128.
  20. 20. Huxman TE, Hamerlynck EP, Loik ME, Smith SD. 1998. Gas exchange and chlorophyll fluorescence responses of three south-western Yucca species to elevated CO2 and high temperature.Plant, Cell & Environment21: 1275–1283.
  21. 21. Chen JP, Burke JJ, Xin ZG. 2010. Role of phosphatidic acid in high temperature tolerance in maize.Crop Science50: 2506–2515.
  22. 22. Eckardt NA, Snyder GW, Portis AR Jr, Ogren WL. 1997. Growth and photosynthesis under high and low irradiance of Arabidopsis thaliana antisense mutants with reduced ribulose-1,5-bisphosphate carboxylase/oxygenase activase content.Plant Physiology113: 575–586.
  23. 23. Crafts-Brandner SJ, Salvucci ME. 2002. Sensitivity of photosynthesis in a C4 plant, maize, to heat stress.Plant Physiology129: 1773–1780.
  24. 24. Chazdon RL. 1988. Sunflecks and their importance to forest understorey plants.Advances in Ecological Research18: 1–63.
  25. 25. Vico G, Manzoni S, Palmroth S, Katul G. 2011. Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes. TheNew Phytologist192: 640–652.
  26. 26. Osterhout WJV, Haas ARC. 1918. On the dynamics of photosynthesis.The Journal of General Physiology1: 1–16.
  27. 27. Walker DA. 1973. Photosynthetic induction phenomena and the light activation of ribulose diphosphate carboxylase.The New Phytologist72: 209–235.
  28. 28. Tang Y, Liang NS. 2000. Characterization of the photosynthetic induction response in a Populus species with stomata barely responding to light changes.Tree Physiol20: 969–976.
  29. 29. Lawson T, Weyers JDB. 1999. Spatial and temporal variation in gas exchange over the lower surface ofPhaseolus vulgarisprimary leaves.Journal of Experimental Botany50: 1381–1391.
  30. 30. Pearcy RW. 1990. Sunflecks and photosynthesis in plant canopies.Annual Review of Plant Physiology and Plant Molecular Biology41: 421–453.
  31. 31. Lawson T, von Caemmerer S, Baroli I. 2010. Photosynthesis and stomatal behaviour. In: Luttge U, Beyschlag W, Budel B, Francis D, eds. Progress in Botany, Vol. 72. Heidelberg: Springer, 265–304.
  32. 32. Lawson T, Blatt MR. 2014. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency.Plant Physiology164: 1556–1570.
  33. 33. Lawson T. 2009. Guard cell photosynthesis and stomatal function. TheNew Phytologist181: 13–34.
  34. 34. Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F, Porée F, Boucherez J, Lebaudy A, Bouchez D, Very AA,. 2003. The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration.Proceedings of the National Academy of Sciences of the United States of America100: 5549–5554.
  35. 35. Suhita D, Raghavendra AS, Kwak JM, Vavasseur A. 2004. Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure.Plant Physiology134: 1536–1545.
  36. 36. Blatt MR, Armstrong F. 1993. K+ channels of stomatal guard cells: abscisic acid-evoked control of the outward rectifier mediated by cytoplasmic pH.Planta191: 330–341.
  37. 37. Grabov A, Blatt MR. 1997. Parallel control of the inward-rectifier K+ channel by cytosolic-free Ca2+ and pH in Vicia guard cells.Planta201: 84–95.
  38. 38. Raschke K, Firn RD, Pierce M. 1975. Stomatal closure in response to xanthoxin and abscisic acid.Planta125: 149–160.
  39. 39. Roelfsema MG, Prins HA. 1995. Effect of abscisic acid on stomatal opening in isolated epidermal strips of abi mutants ofArabidopsis thaliana.Physiologia Plantarum95: 373–378.
  40. 40. Zhang X, Miao YC, An GY, Zhou Y, Shangguan ZP, Gao JF, Song CP. 2001. K+ channels inhibited by hydrogen peroxide mediate abscisic acid signaling inViciaguard cells.Cell Research11: 195–202.
  41. 41. Dow GJ, Bergmann DC, Berry JA. 2014. An integrated model of stomatal development and leaf physiology.The New Phytologist201: 1218–1226.
  42. 42. Hetherington AM, Woodward FI. 2003. The role of stomata in sensing and driving environmental change.Nature424: 901–908.
  43. 43. Franks PJ, Beerling DJ. 2009. CO2-forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic.Geobiology7: 227–236.
  44. 44. Franks PJ, Farquhar GD. 2007. The mechanical diversity of stomata and its significance in gas-exchange control.Plant Physiology143: 78–87.
  45. 45. Drake PL, Froend RH, Franks PJ. 2013. Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance.Journal of Experimental Botany64: 495–505.
  46. 46. Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K. 2008. CO2 regulatorSLAC1 and its homologues are essential for anion homeostasis in plant cells.Nature452: 483–486.
  47. 47. Wang D, Maughan MW, Sun J, Feng X, Miguez F, Lee D, Dietze MC. 2012. Impact of nitrogen allocation on growth and photosynthesis of Miscanthus (Miscanthus × giganteus).GCB Bioenergy4: 688–697.
  48. 48. Merlot S, Leonhardt N, Fenzi F, Valon C, Costa M, Piette L, Vavasseur A, Genty B, Boivin K, Müller A. 2007. Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure.The EMBO Journal26: 3216–3226.
  49. 49. De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H. 2009. Review: CLC-mediated anion transport in plant cells.Philosophical Transactions of the Royal Society B: Biological Sciences364: 195–201.
  50. 50. Gobert A, Isayenkov S, Voelker C, Czempinski K, Maathuis FJM. 2007. The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis.Proceedings of the National Academy of Sciences of the United States of America104: 10726–10731.
  51. 51. Valliyodan B, Nguyen HT. 2006. Understanding regulatory networks and engineering for enhanced drought tolerance in plants.Current Opinion in Biotechnology9: 189–195.
  52. 52. Laanemets K, Wang YF, Lindgren O, Wu J, Nishimura N, Lee S, Caddell D, Merilo E, Brosche M, Kilk K. 2013. Mutations in theSLAC1anion channel slow stomatal opening and severely reduce Kþ uptake channel activity via enhanced cytosolic [Ca2þ] and increased Ca2þ sensitivity of Kþ uptake channels.The New Phytologist197: 88–98.
  53. 53. Berger D, Altmann T. 2000. A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana.Genes & Development14: 1119–1131.
  54. 54. Eisenach C, Chen ZH, Grefen C, Blatt MR. 2012. The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K+ channel activity with vegetative growth.The Plant Journal69, 241–251.
  55. 55. Schlüter U, Muschak M, Berger D, Altmann T .2003. Photosynthetic performance of an Arabidopsis mutant with elevated stomatal density (sdd1-1) under different light regimes.Journal of Experimental Botany54: 867–874.
  56. 56. Tanaka Y, Sugano SS, Shimada T, Hara-Nishimura I. 2013. Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis.The New Phytologist198: 757–764.
  57. 57. Büssis D, von Groll U, Fisahn J, Altmann TA. 2006. Stomatal aperture can compensate altered stomatal density in Arabidopsis thaliana at growth light conditions.Funct Plant Biol33: 1037–1043.
  58. 58. Raven JA. 2002. Selection pressures on stomatal evolution.The New Phytologist153: 371–386.
  59. 59. Wullschleger SD.1993. Biochemical limitations to carbon assimilation in C3 plants – a retrospective analysis of theA/Ci curves from 109 species.Journal of Experimental Botany44: 907–920.
  60. 60. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M. 2005. Assessing the generality of the global leaf trait relationships.The New Phytologist166: 485–496.
  61. 61. Hikosaka K, Shigeno A. 2009. The role of Rubisco and cell walls in the interspecific variation in photosynthetic capacity.Oecologia160, 443–451.
  62. 62. Hikosaka K. 2010. Mechanisms underlying interspecific variation in photosynthetic capacity across wild plant species.Plant Biotechnology27: 223–229.
  63. 63. Lawson T, Kramer DM, Raines CA. 2012. Improving yield by exploiting mechanisms underlying natural variation of photosynthesis.Current Opinion in Biotechnology23: 215–220.
  64. 64. Pettigrew WT. 2004. Cotton genotypic variation in the photosynthetic response to irradiance.Photosynthetica42: 567–571.
  65. 65. Gilbert ME, Zwieniecki MA, Holbrook NM. 2011. Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in 11 soybean genotypes before and during mild drought.Journal of Experimental Botany62: 2875–2887.
  66. 66. Flood PJ, Harbinson J, Aarts MGM. 2011. Natural genetic variation in plant photosynthesis.Trends in Plant Science16: 327–335.
  67. 67. Gu J, Yin X, Stomph T-J, Struik PC. 2014. Can exploiting natural genetic variation in leaf photosynthesis contribute to increasing rice productivity? A simulation analysis.Plant, Cell & Environment37: 22–34.
  68. 68. Hamdani S, Qu M, Xin CP, Li M, Chu C, Govindjee , Zhu XG. 2015. Variations between the photosynthetic properties of elite and landrace Chinese rice cultivars revealed by simultaneous measurements of 820 nm transmission signal and chlorophyll a fluorescence induction.Journal of Plant Physiology177: 128–138.
  69. 69. Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Li W, Lin Z, Buckler ES, Qian Q, Zhang QF, Li J, Han B. 2010. Genome-wide association studies of 14 agronomic traits in rice landraces.Nature Genetics42: 961–967.
  70. 70. Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, Li W, Guo Y, Deng L, Zhu C, Fan D, Lu Y, Weng Q, Liu K, Zhou T, Jing Y, Si L, Dong G, Huang T, Lu T. 2012. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm.Nature Genetics44: 32–40.
  71. 71. Mckown AD, Guy RD, Quamme L, Klapste J, Mantia JL, Constabel CP, El-Kassaby YA, Hamelin RC, Zifkin M, Azam MS. 2014b. Association genetics, geography and ecophysiology link stomatal patterning inPopulus trichocarpawith carbon gain and disease resistance trade-offs.Molecular Ecology23: 5771–5790.
  72. 72. Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F. 2010. Linkage and association mapping of Arabidopsis thaliana flowering time in nature.PLoS Genetics6:e1000940.
  73. 73. Sonah H, O’Donoughue L, Cober E, Rajcan I, Belzile F. 2014. Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soybean.Plant Biotechnology Journal. doi:10.1111/pbi.12249.
  74. 74. Eckert AJ, Dyer RJ. 2012. Defining the landscape of adaptive genetic diversity.Molecular Ecology21: 2836–2838.
  75. 75. Savolainen O, Pyhajarvi T, Knurr T. 2007. Gene flow and local adaptation in trees.Annual Review of Ecology Evolution and Systematics38: 595–619.
  76. 76. Kirschbaum MUF, Gross LJ, Pearcy RW. 1988. Observed and modeled stomatal responses to dynamic light environments in the shade plantAlocasia macrorrhiza.Plant, Cell & Environment11: 111–121.
  77. 77. Zipperlen SW, Press MC. 1997. Photosynthetic induction and stomatal oscillations in relation to the light environment of twodipterocarprain forest tree species.Journal of Ecology85: 491–503.
  78. 78. Naumburg E, Ellsworth DS, Katul GG. 2001. Modeling dynamic understory photosynthesis of contrasting species in ambient and elevated carbon dioxide.Oecologia126: 487–499.
  79. 79. Wang Y, Papanatsiou M, Eisenach C, Karnik R, Williams M, Hills A, Lew VL, Blatt MR. 2012. Systems dynamic modeling of a guard cell Cl- channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration.Plant Physiology160: 1956–1967.
  80. 80. Blatt MR, Wang YZ, Leonhardt N, Hillsa A. 2014. Exploring emergent properties in cellular homeostasis using OnGuard to model K+ and other ion transport in guard cells.Journal of Plant Physiology17: 1770–778.

Written By

Mingnan Qu, Saber Hamdani and James A. Bunce

Submitted: September 9th, 2015 Reviewed: January 11th, 2016 Published: March 30th, 2016