James H. Richards

Hydraulic lift: consequences of water efflux from the roots of plants

Abstract Hydraulic lift is the passive movement of water from roots into soil layers with lower water potential, while other parts of the root system in moister soil layers, usually at depth, are absorbing water. Here, we review the brief history of laboratory and field evidence supporting this phenomenon and discuss some of the consequences of this below-ground behavior for the ecology of plants. Hydraulic lift has been shown in a relatively small number of species (27 species of herbs, grasses, shrubs, and trees), but there is no fundamental reason why it should not be more common as long as active root systems are spanning a gradient in soil water potential (Ψs) and that the resistance to water loss from roots is low. While the majority of documented cases of hydraulic lift in the field are for semiarid and arid land species inhabiting desert and steppe environments, recent studies indicate that hydraulic lift is not restricted to these species or regions. Large quantities of water, amounting to an appreciable fraction of daily transpiration, are lifted at night. This temporary partial rehydration of upper soil layers provides a source of water, along with soil moisture deeper in the profile, for transpiration the following day and, under conditions of high atmospheric demand, can substantially facilitate water movement through the soil-plant-atmosphere system. Release of water into the upper soil layers has been shown to afford the opportunity for neighboring plants to utilize this source of water. Also, because soils tend to dry from the surface downward and nutrients are usually most plentiful in the upper soil layers, lifted water may provide moisture that facilitates favorable biogeochemical conditions for enhancing mineral nutrient availability, microbial processes, and the acquisition of nutrients by roots. Hydraulic lift may also prolong or enhance fine-root activity by keeping them hydrated. Such indirect benefits of hydraulic lift may have been the primary selective force in the evolution of this process. Alternatively, hydraulic lift may simply be the consequence of roots not possessing true rectifying properties (i.e., roots are leaky to water). Finally, the direction of water movement may also be downward or horizontal if the prevailing Ψs gradient so dictates, i.e., inverse, or lateral, hydraulic lift. Such downward movement through the root system may allow growth of roots in otherwise dry soil at depth, permitting the establishment of many phreatophytic species.

Nighttime Stomatal Conductance and Transpiration in C3 and C4 Plants

Incomplete stomatal closure during the night is observed in a diverse range of C3 and C4 species ([Fig. 1][1] ; Supplemental Table S1) and can lead to substantial nighttime transpirational water loss. Although water loss is an inevitable consequence of stomatal opening for photosynthetic carbon gain

Genetics of drought adaptation in Arabidopsis thaliana : I. Pleiotropy contributes to genetic correlations among ecological traits

We examined patterns of genetic variance and covariance in two traits (i) carbon stable isotope ratio δ13C (dehydration avoidance) and (ii) time to flowering (drought escape), both of which are putative adaptations to local water availability. Greenhouse screening of 39 genotypes of Arabidopsis thaliana native to habitats spanning a wide range of climatic conditions, revealed a highly significant positive genetic correlation between δ13C and flowering time. Studies in a range of C3 annuals have also reported large positive correlations, suggesting the presence of a genetically based trade‐off between mechanisms of dehydration avoidance (δ13C) and drought escape (early flowering). We examined the contribution of pleiotropy by using a combination of mutant and near‐isogenic lines to test for positive mutational covariance between δ13C and flowering time. Ecophysiological mutants generally showed variation in δ13C but not flowering time. However, flowering time mutants generally demonstrated pleiotropic effects consistent with natural variation. Mutations that caused later flowering also typically resulted in less negative δ13C and thus probably higher water use efficiency. We found strong evidence for pleiotropy using near‐isogenic lines of FRIGIDA and FLOWERING LOCUS C, cloned loci known to be responsible for natural variation in flowering time. These data suggest the correlated evolution of δ13C and flowering time is explained in part by the fixation of pleiotropic alleles that alter both δ13C and time to flowering.

Magnitude and mechanisms of disequilibrium between predawn plant and soil water potentials

Predawn plant water potential (Ψw, measured with leaf psychrometers) and surrogate measurements made with the pressure chamber (termed Ψpc here) are used to infer comparative ecological performance, based on the expectation that these plant potentials reflect the wettest soil Ψw accessed by roots. There is growing evidence, however, that some species exhibit substantial predawn disequilibrium (PDD), defined as plant Ψw or Ψpc at predawn substantially more negative than the Ψw of soil accessed by roots. In the western Great Basin desert, the magnitude of PDD calculated as soil Ψw minus predawn leaf Ψw was as large as 1.4 and 2.7 MPa for two codominant shrub species, Chrysothamnus nauseosus and Sarcobatus vermiculatus, respectively. The magnitude of PDD calculated as soil Ψw minus predawn Ψpc was smaller, up to 0.6 and 2.1 MPa for Chrysothamnus and Sarcobatus, respectively. For both species, mechanisms contributing to PDD included nighttime transpiration and putative leaf apoplastic solutes, but not hydraul...

Local adaptation across a climatic gradient despite small effective population size in the rare sapphire rockcress

When assigning conservation priorities in endangered species, two common management strategies seek to protect remnant populations that (i) are the most genetically divergent or (ii) possess the highest diversity at neutral genetic markers. These two approaches assume that variation in molecular markers reflects variation in ecologically important traits and ignore the possibility of local adaptation among populations that show little divergence or variation at marker loci. Using common garden experiments, we demonstrate that populations of the rare endemic plant Arabis fecunda are physiologically adapted to the local microclimate. Local adaptation occurs despite (i) the absence of divergence at almost all marker loci and (ii) very small effective population sizes, as evidenced by extremely low levels of allozyme and DNA sequence polymorphism. Our results provide empirical evidence that setting conservation priorities based exclusively on molecular marker diversity may lead to the loss of locally adapted populations.

Genetics of Drought Adaptation in Arabidopsis thaliana II. Qtl Analysis of a New Mapping Population, Kas-1 × Tsu-1

Abstract Despite compelling evidence that adaptation to local climate is common in plant populations, little is known about the evolutionary genetics of traits that contribute to climatic adaptation. A screen of natural accessions of Arabidopsis thaliana revealed Tsu-1 and Kas-1 to be opposite extremes for water-use efficiency and climate at collection sites for these accessions differs greatly. To provide a tool to understand the genetic basis of this putative adaptation, Kas-1 and Tsu-1 were reciprocally crossed to create a new mapping population. Analysis of F3 families showed segregating variation in both δ13C and transpiration rate, and as expected these traits had a negative genetic correlation (rg=− 0.3). 346 RILs, 148 with Kas-1 cytoplasm and 198 with Tsu-1 cytoplasm, were advanced to the F9 and genotyped using 48 microsatellites and 55 SNPs for a total of 103 markers. This mapping population was used for QTL analysis of δ13C using F9 RIL means. Analysis of this reciprocal cross showed a large effect of cytoplasmic background, as well as two QTL for δ13C. The Kas-1 × Tsu-1 mapping population provides a powerful new resource for mapping QTL underlying natural variation and for dissecting the genetic basis of water-use efficiency differences.

Predawn disequilibrium between plant and soil water potentials in two cold-desert shrubs

Abstract Classical water relations theory predicts that predawn plant water potential should be in equilibrium with soil water potential (soil Ψw) around roots, and many interpretations of plant water status in natural populations are based on this expectation. We examined this expectation for two salt-tolerant, cold-desert shrub species in glasshouse experiments where frequent watering assured homogeneity in soil Ψw and soil-root hydraulic continuity and where NaCl controlled soil Ψw. Plant water potentials were measured with a pressure chamber (xylem Ψp) and thermocouple psychrometers (leaf Ψw). Soil Ψw was measured with in situ thermocouple psychrometers. Predawn leaf Ψw and xylem Ψp were significantly more negative than soil Ψw, for many treatments, indicating large predawn soil-plant Ψw disequilibria: up to 1.2 MPa for Chrysothamnus nauseosus (0 and 100 mm NaCl) and 1.8 MPa for Sarcobatus vermiculatus (0, 100, 300, and 600 mm NaCl). Significant nighttime canopy water loss was one mechanism contributing to predawn disequilibrium, assessed by comparison of xylem Ψp for bagged (to minimize transpiration) and unbagged canopies, and by gas exchange measurements. However, nighttime transpiration accounted for only part of the predawn disequilibrium. Other mechanisms that could act with nighttime transpiration to generate large predawn disequilibria are described and include a model of how leaf apoplastic solutes could contribute to the phenomenon. This study is among the first to conclusively document such large departures from the expectation of predawn soil-plant equilibrium for C3 shrubs, and provides a general framework for considering relative contributions of nighttime transpiration and other plant-related mechanisms to predawn disequilibrium.

Physiological Genomics of Response to Soil Drying in Diverse Arabidopsis Accessions

This work examines the physiological and transcriptomic responses to soil drying in 17 diverse accessions of Arabidopsis thaliana, finding that acclimation to drought stress involved increased investment in photosynthesis, carbohydrate turnover, and root growth, as well as activation of abscisic acid signaling pathways and identifying functional variants of key stress response genes. Arabidopsis thaliana, like many species, is characterized by abundant genetic variation. This variation is rapidly being cataloged at the sequence level, but careful dissection of genetic variation in whole-organism responses to stresses encountered in the natural environment are lacking; this functional variation can be exploited as a natural mutant screen to determine gene function. Here, we document physiological and transcriptomic response to soil drying in 17 natural accessions of Arabidopsis. By imposing ecologically realistic stress conditions, we found that acclimation in Arabidopsis involved a strong signature of increased investment in photosynthesis, carbohydrate turnover, and root growth. Our results extend previous work in the Columbia accession suggesting that abscisic acid signaling pathways play an important role in drought stress response. We also identified several mechanisms, including an increase in leaf nitrogen concentration and upregulation of two-component signaling relays, that were common to most natural accessions but had not been identified in studies using only the Columbia accession. Principal component analysis reveals strong correlations between suites of genes and specific physiological responses to stress. The functional variants we identified may represent adaptive mutations in natural habitats and useful variants for agronomic improvement of crop species.

Characterizing genomic variation of Arabidopsis thaliana: the roles of geography and climate

Arabidopsis thaliana inhabits diverse climates and exhibits varied phenology across its range. Although A. thaliana is an extremely well‐studied model species, the relationship between geography, growing season climate and its genetic variation is poorly characterized. We used redundancy analysis (RDA) to quantify the association of genomic variation [214 051 single nucleotide polymorphisms (SNPs)] with geography and climate among 1003 accessions collected from 447 locations in Eurasia. We identified climate variables most correlated with genomic variation, which may be important selective gradients related to local adaptation across the species range. Climate variation among sites of origin explained slightly more genomic variation than geographical distance. Large‐scale spatial gradients and early spring temperatures explained the most genomic variation, while growing season and summer conditions explained the most after controlling for spatial structure. SNP variation in Scandinavia showed the greatest climate structure among regions, possibly because of relatively consistent phenology and life history of populations in this region. Climate variation explained more variation among nonsynonymous SNPs than expected by chance, suggesting that much of the climatic structure of SNP correlations is due to changes in coding sequence that may underlie local adaptation.

Extensive summer water pulses do not necessarily lead to canopy growth of Great Basin and northern Mojave Desert shrubs

Plant species and functionally related species groups from arid and semi-arid habitats vary in their capacity to take up summer precipitation, acquire nitrogen quickly after summer precipitation, and subsequently respond with ecophysiological changes (e.g. water and nitrogen relations, gas exchange). For species that respond ecophysiologically, the use of summer precipitation is generally assumed to affect long-term plant growth and thus alter competitive interactions that structure plant communities and determine potential responses to climate change. We assessed ecophysiological and growth responses to large short-term irrigation pulses over one to three growing seasons for several widespread Great Basin and northern Mojave Desert shrub species: Chrysothamnus nauseosus, Sarcobatus vermiculatus, Atriplex confertifolia, and A. parryi. We compared control and watered plants in nine case studies that encompassed adults of all four species, juveniles for three of the species, and two sites for two of the species. In every comparison, plants used summer water pulses to improve plant water status or increase rates of functioning as indicated by other ecophysiological characters. Species and life history stage responses of ecophysiological parameters (leaf N, δ15N, δ13C, gas exchange, sap flow) were consistent with several previous short-term studies. However, use of summer water pulses did not affect canopy growth in eight out of nine comparisons, despite the range of species, growth stages, and site conditions. Summer water pulses affected canopy growth only for C. nauseosus adults. The general lack of growth effects for these species might be due to close proximity of groundwater at these sites, co-limitation by nutrients, or inability to respond due to phenological canalization. An understanding of the connections between short-term ecophysiological responses and growth, for different habitats and species, is critical for determining the significance of summer precipitation for desert community dynamics.