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Arabis alpina and Arabidopsis thaliana have different stomatal development strategies in response to high altitude pressure conditions

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Abstract

The altitudinal gradient involves changes of the partial pressures of atmospheric gases such as CO2. This omnipresent phenomenon likely represents an evolutionary selective agent. We asked whether high altitude plant species had evolved specific response strategies to cope with high altitude pressure conditions. Plants of the high altitude species Arabis alpina and the low altitude species Arabidopsis thaliana were cultivated in growth chambers with high altitude pressure conditions (corresponding to 3000 m a.s.l.) and low altitude conditions (560 m). In both species, high altitude conditions resulted in the narrowing of stomatal aperture as well as a decrease in leaf area and weight. A. alpina produced significantly more stomata under high altitude conditions compared to low altitude conditions, while A. thaliana did not. Under low altitude conditions, however, stomatal density of A. alpina was smaller compared to A. thaliana. The increase in stomatal density of A. alpina was strongly related to the decrease in the partial pressure of CO2 under high altitude conditions. Thus, the adaptation of the high altitude plant A. alpina to high altitude pressure conditions does not consist in a genetically fixed elevated stomatal density but in a different response strategy of stomatal development to environmental factors compared to the lowland plant A. thaliana. A. alpina developed stomata largely uncoupled from other environmental factors than CO2. The increased stomatal density of A. alpina may ensure an optimal CO2 supply during the periods of favourable weather conditions for photosynthesis that are relatively rare and short in the alpine life zone.

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References

  • Alduchov OE, Eskridge RE (1996) Improved Magnus form approximation of saturation vapour pressure. J Appl Meteorol 35:601–609

    Article  Google Scholar 

  • Belin C, Thomine S, Schroeder JI (2010) Water balance and the regulation of stomatal movements. In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptations in plants: physiological, molecular and genomic foundation. Springer, Dordrecht, pp 283–305

    Google Scholar 

  • Buckley TN (2005) The control of stomata by water balance. New Phytol 168:275–292

    Article  CAS  PubMed  Google Scholar 

  • Büssis D, von Groll U, Fisahn J, Altmann T (2006) Stomatal aperture can compensate altered stomatal density in Arabidopsis thaliana at growth light conditions. Funct Plant Biol 33:1037–1043

    Article  Google Scholar 

  • Casson SA, Hetherington AM (2010) Environmental regulation of stomatal development. Curr Opin Plant Biol 13:90–95

    Article  CAS  PubMed  Google Scholar 

  • Casson SA, Franklin KA, Gray JE, Grierson CS, Whitealm GC, Hetherington AM (2009) Phytochrome B and PIF4 regulate stomatal development in response to light quantitiy. Curr Biol 19:229–234

    Article  CAS  PubMed  Google Scholar 

  • Cowling SA, Sage RF (1998) Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris. Plant, Cell Environ 21:427–435

    Article  CAS  Google Scholar 

  • Easlon HM, Bloom AJ (2014) Easy leaf area: automated digital image analysis for rapid and accurate measurement of leaf area. Appl Plant Sci 2:1400033

    Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • Gale J (1972) Availability of carbon dioxide for photosynthesis at high altitudes: theoretical considerations. Ecology 53:494–497

    Article  Google Scholar 

  • Gerhart LM, Ward JK (2010) Plant responses to low [CO2] of the past. New Phytol 188:674–695

    Article  PubMed  Google Scholar 

  • Greenwood DR, Scarr MJ, Christophel DC (2003) Leaf stomatal frequency in the Australian tropical rainforest tree Neolitsea dealbata (Lauraceae) as a proxy measure of atmospheric pCO2. Palaeogeogr Palaeoclimatol Palaeoecol 196:375–393

    Article  Google Scholar 

  • Hashimoto M, Negi J, Young J, Israelsson M, Schroeder JI, Iba K (2006) Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nat Cell Biol 8:391–397

    Article  CAS  PubMed  Google Scholar 

  • Hess HE, Landolt E, Hirzel R (1970) Flora der Schweiz und angrenzender Gebiete, Band 2, Nymphaeaceae bis Primulaceae. Birkhäuser, Basel

    Google Scholar 

  • Hovenden MJ, Brodribb T (2000) Altitude of origin influences stomatal conductance and therefore maximum assimilation rate in Southern Beech, Nothofagus cunninghamii. Aust J Plant Physiol 27:451–456

    Article  CAS  Google Scholar 

  • Hovenden MJ, Schimanski LJ (2000) Genotypic differences in growth and stomatal morphology of Southern Beech, Nothofagus cunninghamii, exposed to depleted CO2 concentrations. Aust J Plant Physiol 27:281–287

    Article  Google Scholar 

  • Hu H et al (2010) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat Cell Biol 12:87–93

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hu JJ et al (2015) A new positive relationship between pCO2 and stomatal frequency in Quercus guyavifolia (Fagaceae): a potential proxy for palaeo-CO2 levels. Ann Bot 115:777–788

    Article  PubMed  Google Scholar 

  • Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123:32–40

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life, 2nd edn. Springer, Berlin

    Book  Google Scholar 

  • Körner C, Allison A, Hilscher H (1983) Altitudinal variation of leaf diffusive conductance and leaf anatomy in heliophytes of montane New Guinea and their interrelation with microclimate. Flora 174:91–135

    Google Scholar 

  • Körner C, Bannister P, Mark AF (1986) Altitudinal variation in stomatal conductance, nitrogen content and leaf anatomy in different plant life forms in New Zealand. Oecologia 69:577–588

    Article  Google Scholar 

  • Körner C, Neumayer M, Pelaez Menendez-Riedl S, Smeets-Scheel A (1989) Functional morphology of mountain plants. Flora 182:353–383

    Google Scholar 

  • Kouwenberg LLR, Kürschner WM, McElwain JC (2007) Stomatal frequency change over altitudinal gradients: prospects for paleoaltimetry. Rev Mineral Geochem 66:215–241

    Article  CAS  Google Scholar 

  • Masle J (2000) The effects of elevated CO2 concentrations on cell division rates, growth patterns, and blade anatomy in young wheat plants are modulated by factors related to leaf position, vernalization, and genotype. Plant Physiol 122:1399–1415

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Merilo E, Jõesaar I, Brosché M, Kollist H (2014) To open or to close: species-specific responses to simultaneously applied opposing environmental factors. New Phytol 202:499–508

    Article  PubMed  Google Scholar 

  • Morison JIL, Gallouët E, Lawson T, Cornic G, Herbin R, Baker NR (2005) Lateral diffusion of CO2 in leaves is not sufficient to support photosynthesis. Plant Physiol 139:254–266

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mott KA (1990) Sensing of atmospheric CO2 by plants. Plant, Cell Environ 13:731–737

    Article  CAS  Google Scholar 

  • Mott KA, Parkhurst DF (1991) Stomatal responses to humidity in air and helox. Plant, Cell Environ 14:509–515

    Article  Google Scholar 

  • Nagy L, Grabherr G (2009) The biology of alpine habitats. Oxford University Press, Oxford

    Google Scholar 

  • Qiang W et al (2003) Variations in stomatal density and carbon isotope values of Picea crassifolia at different altitudes in the Qilian Mountains. Trees 17:258–262

    Google Scholar 

  • Ranasinghe S, Taylor G (1995) Mechanism for increased leaf growth in elevated CO2. J Exp Bot 47:349–358

    Article  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Rev Palaeobot Palynol 114:1–28

    Article  PubMed  Google Scholar 

  • Royer DL et al (2001) Paleobotanical evidence for near present-day levels of atmospheric CO2 during part of the Tertiary. Science 292:2310–2313

    Article  CAS  PubMed  Google Scholar 

  • Scholl R, Rivero-Lepinckas L, Crist D (1998) Growth of plants and preservation of seeds. In: Martinez-Zapater JM, Salinas J (eds) Arabidopsis protocols. Humana Press, Totowa, pp 1–12

    Chapter  Google Scholar 

  • Skirycz A et al (2011) Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for Ethylene signaling in cell cycle arrest. Plant Cell 23:1876–1888

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smith WK, Geller GN (1979) Plant transpiration at high elevations: theory, field measurements, and comparisons with desert plants. Oecologia 41:109–122

    Article  Google Scholar 

  • Stults DZ, Wagner-Cremer F, Axsmith BJ (2011) Atmospheric paleo-CO2 estimates based on Taxodium distichum (Cupressaceae) fossils from the Miocene and Pliocene of eastern North America. Palaeogeogr Palaeoclimatol Palaeoecol 309:327–332

    Article  Google Scholar 

  • Talbott LD, Rahveh E, Zeiger E (2003) Relative humidity is a key factor in the acclimation of the stomatal response to CO2. J Exp Bot 54:2141–2147

    Article  CAS  PubMed  Google Scholar 

  • Tanaka Y, Sugano SS, Shimada T, Hara-Nishimura I (2013) Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytol 198:757–764

    Article  CAS  PubMed  Google Scholar 

  • Teng N, Wang J, Chen T, Wu X, Wang Y, Lin J (2006) Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytol 172:92–103

    Article  CAS  PubMed  Google Scholar 

  • Terashima I, Masuzawa T, Ohba H, Yokoi Y (1995) Is photosynthesis suppressed at higher elevations due to low CO2 pressure? Ecology 76:2663–2668

    Article  Google Scholar 

  • Vonlanthen C, Bühler A, Veit H, Kammer P, Eugster W (2004) Charakterisierung ökologischer Standortfaktoren in alpinen Pflanzengemeinschaften. Mitt Nat forsch Ges Bern 61:49–77

    Google Scholar 

  • Wang B et al (2012) A novel histidine kinase gene, ZmHK9, mediate drought tolerance through the regulation of stomatal development in Arabidopsis. Gene 501:171–179

    Article  CAS  PubMed  Google Scholar 

  • Ward JK, Kelly JK (2004) Scaling up evolutionary responses to elevated CO2: lessons from Arabidopsis. Ecol Lett 7:427–440

    Article  Google Scholar 

  • Ward JK, Strain BR (1997) Effects of low and elevated CO2 partial pressure on growth and reproduction of Arabidopsis thaliana from different elevations. Plant, Cell Environ 20:254–260

    Article  Google Scholar 

  • Ward JK, Antonovics J, Thomas RB, Strain BR (2000) Is atmospheric CO2 a selective agent on model C3 annuals? Oecologia 123:330–341

    Article  Google Scholar 

  • Woodward FI (1986) Ecophysiological studies on the shrub Vaccinium myrtillus L. taken from a wide altitudinal range. Oecologia 70:580–586

    Article  Google Scholar 

  • Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327:617–618

    Article  Google Scholar 

  • Woodward FI, Bazzaz FA (1988) The responses of stomatal density to CO2 partial pressure. J Exp Bot 39:1771–1781

    Article  Google Scholar 

  • Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytol 131:311–327

    Article  Google Scholar 

  • Woodward FI, Lake JA, Quick WP (2002) Stomatal development and CO2: ecological consequences. New Phytol 153:477–484

    Article  CAS  Google Scholar 

  • Wuyts N, Massonnet C, Dauzat M, Granier C (2012) Structural assessment of the impact of environmental constraints on Arabidopsis thaliana leaf growth: a 3D approach. Plant, Cell Environ 35:1631–1646

    Article  Google Scholar 

  • Xie C et al (2012) Overexpression of MtCAS31 enhances drought tolerance in transgenic Arabidopsis by reducing stomatal density. New Phytol 195:124–135

    Article  CAS  PubMed  Google Scholar 

  • Yoo CY (2010) The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22:4128–4141

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang L, Niu H, Wang S, Zhu X, Luo C, Li Y (2012) Gene or environment? Species-specific control of stomatal density and length. Ecol Evol 2:1065–1070

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank the reviewers for their valuable comments and helpful suggestions on the manuscript. We are grateful to Daniel Braun and Moritz Kammer for laboratory assistance as well as Joel Adler and Lucien Bovet for stimulating discussions. CS was funded by the Swiss National Science Foundation (PA00P3_136474, PZ00P3_148261).

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Correspondence to Peter Manuel Kammer.

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Kammer, P.M., Steiner, J.S. & Schöb, C. Arabis alpina and Arabidopsis thaliana have different stomatal development strategies in response to high altitude pressure conditions. Alp Botany 125, 101–112 (2015). https://doi.org/10.1007/s00035-015-0152-4

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