Advertisement

Journal of Plant Research

, Volume 131, Issue 6, pp 987–999 | Cite as

Dependence of functional traits related to growth rates and their CO2 response on multiple habitat climate factors across Arabidopsis thaliana populations

  • Hiroshi Ozaki
  • Riichi Oguchi
  • Kouki Hikosaka
Regular Paper

Abstract

The values of many plant traits are often different even within a species as a result of local adaptation. Here, we studied how multiple climate variables influence trait values in Arabidopsis thaliana grown under common conditions. We examined 9 climate variables and 29 traits related to vegetative growth rate in 44 global A. thaliana accessions grown at ambient or elevated CO2 concentration ([CO2]) and applied a multiple regression analysis. We found that genetic variations in the traits related to growth rates were associated with various climate variables. At ambient [CO2], plant size was positively correlated with precipitation in the original habitat. This may be a result of larger biomass investment in roots at the initial stage in plants adapting to a lower precipitation. Stomatal conductance and photosynthetic nitrogen use efficiency were negatively correlated with vapor pressure deficit, probably as a result of the trade-off between photosynthetic water- and nitrogen-use efficiency. These results suggest that precipitation and air humidity influence belowground and aboveground traits, respectively. Elevated [CO2] altered climate dependences in some of the studied traits. The CO2 response of relative growth rate was negatively correlated with altitude, indicating that plants inhabiting a higher altitude have less plasticity to changing [CO2]. These results are useful not only for understanding evolutionary process but also to predict the plant species that are favored under future global change.

Keywords

Ecotype Functional traits Global change Growth analysis Habitat filtering Local adaptation 

Notes

Acknowledgements

The authors thank members of the laboratory of plant ecology and functional ecology at Tohoku University for their support in statistical analyses. This work was supported by KAKENHI (nos. 20677001, 21114009, 25291095, 17H03727), Global COE program (J03) and JST CREST Grant number JPMJCR11B3, Japan.

Supplementary material

10265_2018_1058_MOESM1_ESM.pdf (230 kb)
Supplementary material 1 (PDF 230 KB)

References

  1. Akaike H (1974) New look at statistical-model identification. IEEE Trans Autom Control Ac19:716–723Google Scholar
  2. Allen RG, Pereira LS, Raes D, Smith M (1998) Crop evapotranspiration—guidelines for computing crop water requirements. FAO irrigation and drainage paper no. 56. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  3. Atkin OK, Bloomfield KJ, Reich PB, Tjoelker MG et al (2015) Global variability in leaf respiration in relation to climate, plant functional types and leaf traits. New Phytol 206:614–636CrossRefGoogle Scholar
  4. Brachi B, Villoutreix R, Faure N, Hautekèete N, Piquot Y, Pauwels M, Roby D et al (2013) Investigation of the geographical scale of adaptive phenological variation and its underlying genetics in Arabidopsis thaliana. Mol Ecol 22:4222–4240CrossRefGoogle Scholar
  5. Breyne P, Rombaut D, Van Gysel A, Van Montagu M, Gerats T (1999) AFLP analysis of genetic diversity within and between Arabidopsis thaliana ecotypes. Mol Gen Genet 261:627–634CrossRefGoogle Scholar
  6. Cameron AC, Windmeijer FAG (1997) An R-squared measure of goodness of fit for some common nonlinear regression models. J Econometr 77:29–342Google Scholar
  7. Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–126CrossRefGoogle Scholar
  8. Debieu M, Tang C, Stich B, Sikosek T, Effgen S, Josephs E, Schmitt J, Nordborg M, Koornneef M, de Meaux J (2013) Co-variation between seed dormancy, growth rate and flowering time changes with latitude in Arabidopsis thaliana. PLoS One 8:e61075CrossRefGoogle Scholar
  9. Dickie JB, Ellis RH, Ktaak HL, Ryder K, Tompsett PB (1990) Temperature and seed storage longevity. Ann Bot 65:197–204CrossRefGoogle Scholar
  10. Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, González-Martínez SC, Neale DB (2010) Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics 185:969–982CrossRefGoogle Scholar
  11. Field C, Mooney HA (1983) Leaf age and seasonal effects on light, water, and nitrogen use efficiency in a California shrub. Oecologia 56:348–355CrossRefGoogle Scholar
  12. Gamalei YV, van Bel AJE, Pakhomova MV, Sjutkina AV (1994) Effects of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplasmic minor-vein configuration. Planta 194:443–453CrossRefGoogle Scholar
  13. Garnier E (1991) Resource capture, biomass allocation and growth in herbaceous plants. Trend Ecol Evol 6:126–131CrossRefGoogle Scholar
  14. Griffith C, Kim E, Donohue K (2004) Life-history variation and adaptation in the historically mobile plant Arabidopsis thaliana (Brassicaceae) in North America. Am J Bot 91:837–849CrossRefGoogle Scholar
  15. Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary. Am Nat 111:1169–1194CrossRefGoogle Scholar
  16. Hajek P, Kurjak D, von Wühlisch G, Delzon S, Schuldt B (2016) Intraspecific variation in wood anatomical, hydraulic, and foliar traits in ten european beech provenances differing in growth yield. Front Plant Sci 7:791CrossRefGoogle Scholar
  17. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112CrossRefGoogle Scholar
  18. Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Amer Nat 173:579–588CrossRefGoogle Scholar
  19. Heydel F, Cunze S, Bernhardt-Römermann M, Tackenberg O (2014) Long-distance seed dispersal by wind: disentangling the effects of species traits, vegetation types, vertical turbulence and wind speed. Ecol Res 29:641–651CrossRefGoogle Scholar
  20. Hikosaka K, Osone Y (2009) A paradox of leaf-trait convergence: why is leaf nitrogen concentration higher in species with higher photosynthetic capacity? J Plant Res 122:245–251CrossRefGoogle Scholar
  21. Hoch G, Popp M, Körner C (2002) Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos 98:361–374CrossRefGoogle Scholar
  22. Holdridge LR (1947) Determination of world plant formations from simple climatic data. Science 105:367–368CrossRefGoogle Scholar
  23. Hopkins R, Schmitt J, Stinchcombe JR (2008) A latitudinal cline and response to vernalization in leaf angle and morphology in Arabidopsis thaliana (Brassicaceae). New Phytol 179:155–164CrossRefGoogle Scholar
  24. Hunt R (1978) Plant growth analysis. The Institute of Biology’s Studies in Biology Number 96. Edward Arnold, LondonGoogle Scholar
  25. Iio A, Hikosaka K, Anten NPR, Nakagawa Y, Ito A (2014) Global dependence of field-observed leaf area index in woody species on climate: a systematic review. Glob Ecol Biogeogr 23:274–285CrossRefGoogle Scholar
  26. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, New YorkGoogle Scholar
  27. Katabuchi M, Kurokawa H, Davies SJ, Tan S, Nakashizuka T (2012) Soil resource availability shapes community trait structure in a species-rich dipterocarp forest. J Ecol 100:643–651CrossRefGoogle Scholar
  28. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  29. Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921CrossRefGoogle Scholar
  30. Körner C (2003) Alpine plant life: Functional plant ecology of high mountain ecosystems, 2nd edn. Springer, HeidelbergCrossRefGoogle Scholar
  31. Körner C, Diemer M (1987) In situ photosynthetic responses to light, temperature and carbon dioxide in herbaceous plants from low and high altitude. Funct Ecol 1:179–194CrossRefGoogle Scholar
  32. Kraft NJ, Valencia R, Ackerly DD (2008) Functional traits and niche-based tree community assembly in an Amazonian forest. Science 322:580–582CrossRefGoogle Scholar
  33. Lambers H, Poorter H (1992) Inherent variation in growth-rate between higher-plants—a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261CrossRefGoogle Scholar
  34. Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS One 3:e4010CrossRefGoogle Scholar
  35. Li B, Suzuki JI, Hara T (1998) Latitudinal variation in plant size and relative growth rate in Arabidopsis thaliana. Oecologia 115:293–301CrossRefGoogle Scholar
  36. Marquardt DW (1970) Generalized inverses, ridge regression, biased linear estimation and nonlinear estimation. Technometrics 12:591–612CrossRefGoogle Scholar
  37. Moles AT, Perkins SE, Laffan SW, Flores-Moreno H, Awasthy M, Tindall ML, Sack L et al (2014) Which is a better predictor of plant traits: temperature or precipitation? J Veg Sci 25:1167–1180CrossRefGoogle Scholar
  38. Montesinos-Navarro A, Wig J, Pico FX, Tonsor SJ (2011) Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude. New Phytol 189:282–294CrossRefGoogle Scholar
  39. Nagano S, Nakano T, Hikosaka K, Murata E (2013) Pinus pumila photosynthesis is suppressed by water stress in a wind-exposed mountain site. Arct Antarct Alp Res 45:229–237CrossRefGoogle Scholar
  40. Nakamura I, Onoda Y, Matsushima N, Yokoyama J, Kawata M, Hikosaka K (2011) Phenotypic and genetic differences in a perennial herb across a natural gradient of CO2 concentration. Oecologia 165:809–818CrossRefGoogle Scholar
  41. New M, Hulme M, Jones P (1999) Representing twentieth-century space–time climate variability. Part I: development of a 1961–90 mean monthly terrestrial climatology. J Clim 12:829–856CrossRefGoogle Scholar
  42. Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P et al (2010) Plant phenotypic plasticity in a changing climate. Trend Plant Sci 15:684–692CrossRefGoogle Scholar
  43. Oguchi R, Ozaki H, Hanada K, Hikosaka K (2016) Which plant trait explains the variations in relative growth rate and its response to elevated carbon dioxide concentration among Arabidopsis thaliana ecotypes derived from a variety of habitats? Oecologia 180:865–876CrossRefGoogle Scholar
  44. Onoda Y, Hirose T, Hikosaka K (2009) Does leaf photosynthesis adapt to CO2-enriched environments? An experiment on plants originating from three natural CO2 springs. New Phytol 182:698–709CrossRefGoogle Scholar
  45. Pitcairn CER, Grace J (1982) The effect of wind and a reduced supply of phosphorus and nitrogen on the growth and water relations of Festuca arundinacea Schreb. Ann Bot 49:649–660CrossRefGoogle Scholar
  46. Pitcairn CER, Grace J (1984) The effect of wind on provenances of Molinia caerulea L. Ann Bot 54:135–143CrossRefGoogle Scholar
  47. Poorter H, Navas ML (2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol 157:175–198CrossRefGoogle Scholar
  48. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588CrossRefGoogle Scholar
  49. Poorter H, Niinemets Ü, Walter A, Fiorani F, Schurr U (2010) A method to construct dose–response curves for a wide range of environmental factors and plant traits by means of a meta-analysis of phenotypic data. J Exp Bot 61:2043–2055CrossRefGoogle Scholar
  50. Samis KE, Murren CJ, Bossdorf O, Donohue K, Fenster CB, Malmberg RL, Purugganan MD, Stinchcombe JR (2012) Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana. Ecol Evol 2:1162–1180CrossRefGoogle Scholar
  51. Sierra-Almeida A, Cavieres LA, Bravo LA (2009) Freezing resistance varies within the growing season and with elevation in high-Andean species of central Chile. New Phytol 182:461–469CrossRefGoogle Scholar
  52. Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci USA 101:4712–4717CrossRefGoogle Scholar
  53. Taschler D, Beikircher B, Neuner G (2003) Frost resistance and ice nucleation in leaves of five woody timberline species measured in situ during shoot expansion. Tree Physiol 24:331–337CrossRefGoogle Scholar
  54. Tonsor SJ, Scheiner SM (2007) Plastic trait integration across a CO2 gradient in Arabidopsis thaliana. Amer Nat 169:E119–E140CrossRefGoogle Scholar
  55. Valladares F, Sanchez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116CrossRefGoogle Scholar
  56. Valladares F, Gianoli E, Gómez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763CrossRefGoogle Scholar
  57. Wang QW, Nagano S, Ozaki H, Morinaga SI, Hidema J, Hikosaka K (2016) Functional differentiation in UV-B-induced DNA damage and growth inhibition between highland and lowland ecotypes of two Arabidopsis species. Environ Exp Bot 131:110–119CrossRefGoogle Scholar
  58. 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 20:254–260CrossRefGoogle Scholar
  59. Ward JK, Antonovics J, Thomas RB, Strain BR (2000) Is atmospheric CO2 a selective agent on model C3 annuals? Oecologia 123:330–341CrossRefGoogle Scholar
  60. Warren CR, Adams MA (2005) What determines interspecific variation in relative growth rate of Eucalyptus seedlings? Oecologia 144:373–381CrossRefGoogle Scholar
  61. Weinig C, Gravuer KA, Kane NC, Schmitt J (2004) Testing adaptive plasticity to UV: costs and benefits of stem elongation and light-induced phenolics. Evolution 58:2645–2655CrossRefGoogle Scholar
  62. Wolff E, Kull C, Chappellaz J, Fischer H, Miller H, Stocker TF, Watson AJ et al (2005) Modeling past atmospheric CO2: results of a challenge. Eos Trans Am Geophys Union 86:341–345CrossRefGoogle Scholar
  63. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefGoogle Scholar
  64. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W et al (2005) Modulation of leaf economic traits and trait relationships by climate. Glob Ecol Biogeogr 14:411–421CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  2. 2.School of Life SciencesTokyo University of Pharmacy and Life SciencesHachiojiJapan

Personalised recommendations