Abstract
Soil moisture is a key factor affecting plant abundance and distribution, both across and within species. In response to water limitation, plants have evolved numerous morphological, physiological, and phenological adaptations. In both well-watered and water-limited conditions, we identified considerable natural variation in drought-related whole-plant and leaf-level traits among closely related members of the Mimulus guttatus species complex that occupy a diversity of habitats in the field. The self-fertilizing Mimulus nasutus and serpentine-endemic Mimulus nudatus demonstrated the overall greatest tolerance to soil water limitation, exhibiting the smallest reduction in seed set relative to well-watered conditions. This may be due in part to early flowering, faster fruit development, and low stomatal density. In contrast, flowering of coastal M. guttatus was so delayed that it precluded any seed production in water-limited conditions. This range of phenotypic responses to soil water deficit in Mimulus, coupled with developing genomic resources, holds considerable promise for identifying genomic variation responsible for adaptive responses to soil water availability.
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References
Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR, Sandquist DR, Geber MA, Evans AS, Dawson TE, Lechowicz MJ (2000) The evolution of plant ecophysiological traits: recent advances and future directions. BioScience 50:979–995
Angert AL, Huxman TE, Barron-Gafford GA, Gerst KL, Venable DL (2007) Linking growth-strategies to long-term population dynamics in a guild of desert annuals. J Ecol 95:321–331
Araus JL, Slafer GA, Reynolds MP, Royo C (2002) Plant breeding and drought in C3 cereals: what should we breed for? Ann Bot 89:925–940
Arntz AM, Delph LF (2001) Pattern and process: evidence for the evolution of photosynthetic traits in natural populations. Oecologia 127:455–467
Barr HD, Weatherley PE (1962) A reexamination of the relative turgidity technique for estimating water deficit in leaves. Aust J Biol Sci 15:413–428
Bazzaz FA (1979) Physiological ecology of plant succession. Annu Rev Ecol Syst 10:351–371
Beardsley PM, Schoenig SE, Whittall JB, Olmstead RG (2004) Patterns of evolution in western North American Mimulus (Phrymaceae). Am J Bot 91:474–489
Campbell DR, Galen C, Wu CA (2005) Ecophysiology of first and second generation hybrids in a natural plant hybrid zone. Oecologia 144:214–225
Canadell JG, Pataki DE, Pitelka LF (eds) (2007) Terrestrial ecosystems in a changing World. Springer, Berlin
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought––from genes to the whole plant. Funct Plant Biol 30:239–264
Clausen J, Keck DD, Hiesey WM (1940) Experimental studies on the nature of species. I. Effects of varied environments on western North American plants. Carnegie Institute of Washington publication no. 520. Carnegie Institute, Washington
Corbin JD, Thomsen MA, Dawson TE, D’Antonio CM (2005) Summer water use by California coastal prairie grasses: fog, drought, and community composition. Oecologia 145:511–521
Cornwell WK, Grubb PJ (2003) Regional and local patterns in plant species richness with respect to resource availability. Oikos 100:417–428
Culley TM, Dunbar-Wallis AK, Sakai AK, Weller SG, Mishio M, Campbell DR, Herzenach M (2006) Genetic variation of ecophysiological traits in two gynodioecious species of Schiedea (Caryophyllaceae). New Phytol 169:589–601
Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in box elder, Acer negundo. Ecology 74:798–815
Dudley SA (1996) Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50:92–102
Eckhart VM, Geber MA, McGuire C (2004) Experimental studies of selection and adaptation in Clarkia xantiana (Onagraceae). I. Sources of phenotypic variation across a subspecies border. Evolution 58:59–70
Ehleringer JR (1993) Carbon and water relations in desert plants: and isotopic perspective. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon–water relations. Academic Press, San Diego, pp 155–172
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537
Fishman L, Willis JH (2008) Pollen limitation and natural selection on floral characters in the yellow monkeyflower, Mimulus guttatus. New Phytol 177:802–810
Fishman L, Kelly AJ, Willis JH (2002) Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution 56:2138–2155
Fox GA (1990) Drought and the evolution of flowering time in desert annuals. Am J Bot 77:1508–1518
Franke DM, Ellis AG, Dharjwa M, Freshwater M, Padron A, Weis AE (2006) A steep cline in flowering time for Brassica rapa in Southern California: population-level variation in the field and the greenhouse. Int J Plant Sci 167:83–92
Gardner M, Macnair M (2000) Factors affecting the co-existence of the serpentine endemic Mimulus nudatus Curran and its presumed progenitor, Mimulus guttatus Fischer ex DC. Biol J Linn Soc Lond 69:443–459
Garnier E, Cordonnier P, Guillerm JL, Sonié L (1997) Specific leaf area and leaf nitrogen concentration in annual and perennial grass species growing in Mediterranean old-fields. Oecologia 111:490–498
Geber MA, Dawson TE (1990) Genetic variation in and covariation between leaf gas exchange, morphology, and development in Polygonum arenastrum, an annual plant. Oecologia 85:153–158
Geber MA, Dawson TE (1997) Genetic variation in stomatal and biochemical limitations to photosynthesis in the annual plant, Polygonum arenastrum. Oecologia 109:535–546
Gottlieb LD (2003) Rethinking classic examples of recent speciation in plants. New Phytol 161:71–82
Hall MC, Willis JH (2006) Divergent selection on flowering time contributes to local adaptation in Mimulus guttatus populations. Evolution 60:2466–2477
Hausman NJ, Juenger TE, Sen S, Stowe KA, Dawson TE, Simms EL (2005) Quantitative trait loci affecting δ13C and response to differential water availability in Arabidopsis thaliana. Evolution 59:81–96
Heschel MS, Riginos C (2005) Mechanisms of selection for drought stress tolerance and avoidance in Impatiens capensis. Am J Bot 92:37–44
Heschel MS, Donohue K, Hausmann N, Schmitt J (2002) Population differentiation and natural selection for water-use efficiency in Impatiens capensis (Balsaminaceae). Int J Plant Sci 163:907–912
Heschel MS, Sultan SE, Glover S, Sloan D (2004) Population differentiation and plastic responses to drought stress in the generalist annual, Impatiens capensis. Oecologia 139:487–494
Hughes R, Bachmann K, Smirnoff N, Macnair M (2001) The role of drought tolerance in serpentine tolerance in the Mimulus guttatus Fischer ex DC complex. S Afr J Sci 97:581–586
Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403
Juenger TE, McKay J, Hausmann N, Keurentjes JJB, Sen S, Stowe KA, Dawson TE, Simms EL, Richards JH (2005) Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: δ13C, stomatal conductance and transpiration efficiency. Plant Cell Environ 28:697–708
Kiang YT, Hamrick JL (1978) Reproductive isolation in the Mimulus guttatus–M. nasutus complex. Am Midl Nat 100:269–276
Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172
Lambers H, Chapin FS, Pons TL (1998b) Plant physiological ecology. Springer, New York
Li Y, Johnson DA, Su Y, Cui J, Zhang T (2005) Specific leaf area and leaf dry matter content of plants growing in sand dunes. Bot Bull Acad Sin 46:127–134
Lowry DB, Rockwood RC, Willis JH (2008) Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution 62:2196–2214
Lowry DB, Hall MC, Salt DE, Willis JH (2009) Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytol. doi:10.1111/j.1469-8137.209.02901.x
Ludlow MM (1989) Strategies of response to water stress. In: Kreeb KH, Richter H, Minckley TM (eds) Structural and functional responses to environmental stress. SPB Academic, Amsterdam
Ludwig F, Rosenthal DM, Johnston JA, Kane NC, Gross BL, Lexer C, Rieseberg LH, Donovan LA (2004) Selection on leaf ecophysiological traits in a desert hybrid Helianthus species and early-generation hybrids. Evolution 58:2682–2692
Macnair MR, Gardner M (1998) The evolution of edaphic endemics. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 157–171
Maggio A, Zhu J, Hasegawa PM, Bressan RA (2006) Osmogenetics: Aristotle to Arabidopsis. Plant Cell 18:1542–1557
Martin NH, Willis JH (2007) Barriers to gene flow between the monkeyflowers Mimulus guttatus, M. nasutus and their hybrids. Evolution 61:68–82
Masle J, Gilmore SR, Garquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436:866–870
McKay JK, Bishop JG, Lin JZ, Sala A, Richards JH, Mitchell-Olds T (2001) Local adaptation across a climatic gradient despite small effective population size in the rare sapphire rockcress. Proc R Soc Lond B Biol Sci 268:1715–1721
McKay JK, Richeards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana. I. Pleiotropy contributes to genetic correlations among ecological traits. Mol Ecol 12:1137–1151
Mckay JK, Richards JH, Nemali KS, Sen S, Mitchel-Olds T, Boles S, Stahl EA, Wayne T, Juenger TE (2008) Genetics of drought adaptation in Arabidopsis thaliana. II. QTL analysis of a new mapping population, Kas-1 X Tsu-1. Evolution 62:3014–3026
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Murren CJ, Douglass L, Gibson A, Dudash MR (2006) Individual and combined effects of Ca/Mg ratio and water on trait expression in Mimulus guttatus. Ecology 87:2591–2606
Nagy ES, Rice KJ (1997) Local adaptation in two subspecies of an annual plant: implications for migration and gene flow. Evolution 51:1079–1089
Pennell FW (1947) Some hitherto undescribed Scrophulariaceae of the Pacific states. Proc Acad Nat Sci 99:151–171
Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588
Reid CD, Maherali H, Johnson HB, Smith SD (2003) On the relationship between stomatal characters and atmospheric CO2. Geophys Res Lett 30: art. no. 1983
Sakai AK, Weller SG, Wagner WL, Nepokroeff M, Culley TM (2006) Adaptive radiation and evolution of breeding systems in Schiedea (Caryophyllaceae), and endemic Hawaiian genus. Ann Mo Bot Gard 93:49–63
Schulze ED (1986) Carbon dioxide and water vapor exchange in response to drought in the atmosphere and in the soil. Annu Rev Plant Physiol Plant Mol Biol 37:247–274
Sherrard ME, Maherali H (2006) The adaptive significance of drought escape in Avena barbata, an annual grass. Evolution 60:2478–2489
Simpson CG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296:285–289
Stanton ML, Roy BA, Thiede DA (2000) Evolution in stressful environments. I. Phenotypic variability, phenotypic selection, and response to selection in five distinct environmental stresses. Evolution 54:93–111
Turesson G (1922) The genotypic response of the plant species to habitat. Hereditas 3:211–350
Vickery RK (1978) Case studies in the evolution of species complexes in Mimulus. Evol Biol 11:405–507
Weinig C, Ungerer MC, Dorn LA, Kane NC, Toyonaga Y, Halldorsdottir SS, Mackay TFC, Purugganan MD, Schmitt J (2002) Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics 162:1875–1884
Wu CA, Lowry DB, Cooley AM, Wright KM, Lee YW, Willis JH (2008) Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100:220–230
Yu H, Chen X, Hong Y-Y, Wang Y, Xu P, Ke S-D, Liu H-Y, Zhu J-K, Oliver DJ, Xiang C-B (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20:1134–1151
Acknowledgments
We thank Meg Peterson, Calvin Sheng, Eugene Wu, and Mike Yan for assistance at various stages of the experiments, Chantal Reid for discussions of plant physiology, Diane Campbell for statistical advice, and two anonymous reviewers for comments that improved this manuscript. This work was funded by the National Science Foundation though FIBR Grant EF-0328636, Doctoral Dissertation Improvement Grant DEB-0710094, and Environmental Genomics Grant EF-0723814.
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Communicated by Todd Dawson.
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Wu, C.A., Lowry, D.B., Nutter, L.I. et al. Natural variation for drought-response traits in the Mimulus guttatus species complex. Oecologia 162, 23–33 (2010). https://doi.org/10.1007/s00442-009-1448-0
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DOI: https://doi.org/10.1007/s00442-009-1448-0