skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Pinpointing the causal influences of stomatal anatomy and behavior on minimum, operational, and maximum leaf surface conductance
Abstract Leaf surface conductance to water vapor and CO2 across the epidermis (gleaf) strongly determines the rates of gas exchange. Thus, clarifying the drivers of gleaf has important implications for resolving the mechanisms of photosynthetic productivity and leaf and plant responses and tolerance to drought. It is well recognized that gleaf is a function of the conductances of the stomata (gs) and of the epidermis + cuticle (gec). Yet, controversies have arisen around the relative roles of stomatal density (d) and size (s), fractional stomatal opening (α; aperture relative to maximum), and gec in determining gleaf. Resolving the importance of these drivers is critical across the range of leaf surface conductances, from strong stomatal closure under drought (gleaf,min), to typical opening for photosynthesis (gleaf,op), to maximum achievable opening (gleaf,max). We derived equations and analyzed a compiled database of published and measured data for approximately 200 species and genotypes. On average, within and across species, higher gleaf,min was determined 10 times more strongly by α and gec than by d and negligibly by s; higher gleaf,op was determined approximately equally by α (47%) and by stomatal anatomy (45% by d and 8% by s), and negligibly by gec; and higher gleaf,max was determined entirely by d. These findings clarify how diversity in stomatal functioning arises from multiple structural and physiological causes with importance shifting with context. The rising importance of d relative to α, from gleaf,min to gleaf,op, enables even species with low gleaf,min, which can retain leaves through drought, to possess high d and thereby achieve rapid gas exchange in periods of high water availability.  more » « less
Award ID(s):
2017949 1943583 2307341
PAR ID:
10538638
Author(s) / Creator(s):
; ; ; ; ; ; ;
Publisher / Repository:
Plant Physiology
Date Published:
Journal Name:
Plant Physiology
ISSN:
0032-0889
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ABSTRACT Identifying the physiological mechanisms by which plants are adapted to drought is critical to predict species responses to climate change. We measured the responses of leaf hydraulic and stomatal conductances (Kleafandgs, respectively) to dehydration, and their association with anatomy, in seven species of CaliforniaCeanothusgrown in a common garden, including some of the most drought‐tolerant species in the semi‐arid flora. We tested for matching of maximum hydraulic supply and demand and quantified the role of decline ofKleafin driving stomatal closure. AcrossCeanothusspecies, maximumKleafandgswere negatively correlated, and bothKleafandgsshowed steep declines with decreasing leaf water potential (i.e., a high sensitivity to dehydration). The leaf water potential at 50% decline ingswas linked with a low ratio of maximum hydraulic supply to demand (i.e., maximumKleaf:gs). This sensitivity ofgs, combined with low minimum epidermal conductance and water storage, could contribute to prolonged leaf survival under drought. The specialized anatomy of subg.Cerastesincludes trichomous stomatal crypts and pronounced hypodermis, and was associated with higher water use efficiency and water storage. Combining our data with comparative literature of other California species, species of subg. Cerastesshow traits associated with greater drought tolerance and reliance on leaf water storage relative to other California species. In addition to drought resistance mechanisms such as mechanical protection and resistance to embolism, drought avoidance mechanisms such as sensitive stomatal closure could contribute importantly to drought tolerance in dry‐climate adapted species. 
    more » « less
  2. Summary A prevailing hypothesis posits that achieving higher maximum rates of leaf carbon gain and water loss is constrained by geometry and/or selection to limit the allocation of epidermal area to stomata (fS). Under this ‘stomatal‐area minimization hypothesis’, highergs,maxis associated with greater numbers of smaller stomata because this trait combination increasesgs,maxwith minimal increase infS, leading to relative conservation offSsemi‐independent ofgs,maxdue to coordination in stomatal size, density, and pore depth. An alternative hypothesis is that the evolution of highergs,maxcan be enabled by a greater epidermal area allocated to stomata, leading to positive covariation betweenfSandgs,max; we call this the ‘stomatal‐area adaptation hypothesis’. Under this hypothesis, the interspecific scaling betweengs,max, stomatal density, and stomatal size is a by‐product of selection on a moving optimalgs,max.We integrated biophysical and evolutionary quantitative genetic modeling with phylogenetic comparative analyses of a global data set of stomatal density and size from 2408 vascular forest species. The models present specific assumptions of both hypotheses and deduce predictions that can be evaluated with our empirical analyses of forest plants.There are three main results. First, neither the stomatal‐area minimization nor adaptation hypothesis is sufficient to be supported. Second, estimates of interspecific scaling from common regression methods cannot reliably distinguish between hypotheses when stomatal size is bounded. Third, we reconcile both hypotheses with the data by including an additional assumption that stomatal size is bounded by a wide range and under selection; we refer to this synthetic hypothesis as the ‘stomatal adaptation + bounded size’ hypothesis.This study advances our understanding of scaling between stomatal size and density by mathematically describing specific assumptions of competing hypotheses, demonstrating that existing hypotheses are inconsistent with observations, and reconciling these hypotheses with phylogenetic comparative analyses by postulating a synthetic model of selection ongs,max,fS, and stomatal size. 
    more » « less
  3. Abstract Plants differ widely in how soil drying affects stomatal conductance (gs) and leaf water potential (ψleaf), and in the underlying physiological controls. Efforts to breed crops for drought resilience would benefit from a better understanding of these mechanisms and their diversity. We grew 12 diverse genotypes of common bean (Phaseolus vulgarisL.) and four of tepary bean (P. acutifolius;a highly drought resilient species) in the field under irrigation and post‐flowering drought, and quantified responses ofgsandψleaf, and their controls (soil water potential [ψsoil], evaporative demand [Δw] and plant hydraulic conductance [K]). We hypothesised that (i) common beans would be more “isohydric” (i.e., exhibit strong stomatal closure in drought, minimisingψleafdecline) than tepary beans, and that genotypes with largerψleafdecline (more “anisohydric”) would exhibit (ii) smaller increases in Δw, due to less suppression of evaporative cooling by stomatal closure and hence less canopy warming, but (iii) largerKdeclines due toψleafdecline. Contrary to our hypotheses, we found that half of the common bean genotypes were similarly anisohydric to most tepary beans; canopy temperature was cooler in isohydric genotypes leading to smaller increases in Δwin drought; and that stomatal closure andKdecline were similar in isohydric and anisohydric genotypes.gsandψleafwere virtually insensitive to drought in one tepary genotype (G40068). Our results highlight the potential importance of non‐stomatal mechanisms for leaf cooling, and the variability in drought resilience traits among closely related crop legumes. 
    more » « less
  4. Abstract Drought resistance is essential for plant production under water‐limiting environments. Abscisic acid (ABA) plays a critical role in stomata but its impact on hydraulic function beyond the stomata is far less studied. We selected genotypes differing in their ability to accumulate ABA to investigate its role in drought‐induced dysfunction. All genotypes exhibited similar leaf and stem embolism resistance regardless of differences in ABA levels. Their leaf hydraulic resistance was also similar. Differences were only observed between the two extreme genotypes:sitiens(sit; a strong ABA‐deficient mutant) andsp12(a transgenic line that constitutively overaccumulates ABA), where the water potential inducing 50% embolism was 0.25 MPa lower insp12than insit. Maximum stomatal and minimum leaf conductances were considerably lower in plants with higher ABA (wild type [WT] andsp12) than in ABA‐deficient mutants. Variations in gas exchange across genotypes were associated with ABA levels and differences in stomatal density and size. The lower water loss in plants with higher ABA meant that lethal water potentials associated with embolism occurred later during drought insp12plants, followed by WT, and then by the ABA‐deficient mutants. Therefore, the primary pathway by which ABA enhances drought resistance is via declines in water loss, which delays dehydration and hydraulic dysfunction. 
    more » « less
  5. Stomatal closure limits transpiration during drought, restricting water potential decline and delaying the onset of embolism. While critical for ensuring survival during drought, the mechanisms driving stomatal closure during drought remain equivocal. The hormone abscisic acid (ABA) will close stomata in seed plants and is synthesized as leaf turgor declines. ABA driven stomatal closure during drought is particularly apparent in species that are more isohydric. In contrast, in species that have a more anisohydric response to drought, like Fagus sylvatica, the importance of ABA in driving stomatal closure during drought is often overlooked or excluded, in place of a hypothesized passive, water potential driven stomatal closure. Here we investigated whether ABA drives stomata closure during a mid-summer drought in field grown F. sylvatica. We found that as leaf water potential declines during a drought, foliage abscisic acid (ABA) levels increase considerably and stomata close. ABA levels in leaves increase as water potentials decline to within 0.3 MPa of turgor loss point, when stomata close. Foliage ABA levels correlate with stomatal conductance throughout a drought and post-drought period. From these results we argue that it is hard to exclude increased ABA levels driving stomatal closure during drought in the anisohydric species F. sylvatica. 
    more » « less