Skip to main content

Advertisement

Log in

Phenotypic variation between high and low elevation populations of Rumex nepalensis in the Himalayas is driven by genetic differentiation

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Rumex nepalensis, one of several plant species distributed across wide elevation gradient in Himalayas, was studied for difference in seed traits, phenology and photosynthetic characteristics in four populations from 800 m (sub-tropical population: SP), 1300 m (sub-temperate population: STP), 2200 m (temperate population: TP) and 4000 m (alpine population: AP) elevations above mean sea level. Seeds of AP were larger in size and germinated faster at 15 °C than at 25 °C compared to those from lower elevations. Seed raised four populations of the species studied under ex situ conditions of greenhouse showed that AP emerged late but was able to complete its post flowering phenophases much earlier, such that its life cycle was reduced by 14 days compared to SP. Ex-situ and in situ studies in the native habitat for all populations showed AP and SP to differed significantly in most of the photosynthetic traits, thus indicating the two populations to be genetically different. Further studies are required to understand how different genotypes of R. nepalensis would respond to atmospheric warming.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

C i :

Intercellular CO2 concentration

Chl:

Chlorophyll

ECU:

Efficiency of carbon uptake

g S :

Stomatal conductance

PPFD:

Photosynthetic photon flux density

P N :

Net photosynthetic rate

References

  • Anderson JT, Inouye DW, McKinney AM, Colautti RI, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc Biol Sci 279:3843–3852

    Article  PubMed  PubMed Central  Google Scholar 

  • Arft AM, Walker MD, Gurevitch JEA, Alatalo JM, Bret-Harte MS, Dale M, Hollister RD (1999) Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment. Ecol Monograph 69:491–511

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baythayong BS (2011) Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: selection favors adaptive plasticity in fine-grained environments. Am Nat 178(75):87

    Google Scholar 

  • Biere A (1991) Parental effects in Lychnis floscuculi. I Seed size, germination and seedling performance in a controlled environment. J Evol Biol 4:447–465

    Article  Google Scholar 

  • Björkman O (1981) Responses to different quantum flux densities. In: Lange OL, Nobel PS, Osmond CB, Zeigler H (eds) Encyclopedia of Plant Physiology. Springer, Berlin, pp 57–107

    Google Scholar 

  • Booth TH, Nix HA, Busby JR, Hutchinson MF (2014) Bioclim: the first species distribution modelling package, its early applications and relevance to most current MaxEnt studies. Divers Distrib 20:1–9

    Article  Google Scholar 

  • Bosiö J, Stiegler C, Johansson M, Mbufong HN, Christensen TR (2014) Increased photosynthesis compensates for shorter growing season in subarctic tundra-8 years of snow accumulation manipulations. Clim Change 127:321–334

    Article  Google Scholar 

  • Bradley NL, Leopold AC, Ross J, Huffaker W (1999) Phenological changes reflect climate change in Wisconsin. Proc Natl Acad Sci USA 96:9701–9704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bresson CC, Kowalski AS, Kremer A, Delzon S (2009) Evidence of altitudinal increase in photosynthetic capacity: gas exchange measurements at ambient and constant CO2 partial pressures. Ann For Sci 66:505

    Article  Google Scholar 

  • Busby JR (1991) BIOCLIM- a bioclimate analysis and prediction system. In: Margules C, Austin M (eds) Nature conservation: cost effective biological surveys and data analysis. CSIRO, Canberra, pp 64–68

    Google Scholar 

  • Cavender-Bares J, Kozak K, Fine P, Kembel S (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715

    Article  PubMed  Google Scholar 

  • Churkina G, Schimel D, Braswell BH, Xiao XM (2005) Spatial analysis of growing season length control over net ecosystem exchange. Glob Change Biol 11:1777–1787

    Article  Google Scholar 

  • Coate JE, Powell AF, Owens TG, Doyle JJ (2013) Transgressive physiological and transcriptomic responses to light stress in allopolyploid Glycine dolichocarpa (Leguminosae). Heredity 110:160–170

    Article  CAS  PubMed  Google Scholar 

  • Cordell S, Goldstein G, Mueller-Dombois D, Webb D, Vitousek PM (1998) Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity. Oecologia 113:188–196

    Article  CAS  PubMed  Google Scholar 

  • Crawford RMM (2008) Cold climate plants in a warmer world. Plant Ecol Divers 1:285–297

    Article  Google Scholar 

  • Damerval C, De Vienne D, Zivy M, Thiellement H (1986) Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7:52–54

    Article  CAS  Google Scholar 

  • De Frenne P, Graae BJ, Brunet J, Shevtsova A, De Schrijver A, Chabrerie O, Heinken T (2012) The response of forest plant regeneration to temperature variation along a latitudinal gradient. Ann Bot 109:1037–1046

    Article  PubMed  PubMed Central  Google Scholar 

  • DeLucia EH, Berlyn GP (1984) The effect of increasing elevation on leaf cuticle thickness and cuticular transpiration in balsam fir. Can J Bot 62:2423–2431

    Article  Google Scholar 

  • Doley D (1981) Tropical and subtropical forests and woodlands. In: Kozlowski TT (ed) Water deficits and plant growth, vol vol VI. Academic Press, New York, pp 209–323

    Google Scholar 

  • Farooq U, Pandith SA, Saggoo MIS, Lattoo SK (2013) Altitudinal variability in anthraquinone constituents from novel cytotypes of Rumex nepalensis Spreng—a high value medicinal herb of North Western Himalayas. Ind Crop Prod 50:112–117

    Article  CAS  Google Scholar 

  • Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691

    Article  CAS  PubMed  Google Scholar 

  • Frei ES, Scheepens JF, Armbruster GFJ, Stöcklin J (2012) Phenotypic differentiation in a common garden reflects the phylogeography of a widespread Alpine plant. J Ecol 100:297–308

    Article  Google Scholar 

  • Geng Y, Pan X, Xu CY, Zhang WJ, Li B, Chen JK, Lu BR, Song ZP (2007) Phenotypic plasticity rather than locally adapted ecotypes allow the invasive alligator weed to colonize a wide range of habitats. Biol Invasions 9:245–256

    Article  Google Scholar 

  • Haggerty BP, Galloway LF (2011) Response of individual components of reproductive phenology to growing season length in a monocarpic herb. J Ecol 99:242–253

    Article  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908

    Article  CAS  PubMed  Google Scholar 

  • Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18:605–618

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jeong SJ, Ho CH, Gim HJ, Brown ME (2011) Phenology shifts at start vs end of growing season in temperate vegetation over the Northern Hemisphere for the period 1982–2008. Global Change Biol 17:2385–2399

    Article  Google Scholar 

  • Körner C (1999) Alpine plant life. Springer, Berlin

    Book  Google Scholar 

  • 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 1:179–194

    Article  Google Scholar 

  • Körner C, Diemer M (1994) Evidence that plants from high altitudes retains their greater photosynthetic efficiency under elevated CO2. Funct Ecol 8:58–68

    Article  Google Scholar 

  • Körner C, Mayr R (1981) Stomatal behaviour in alpine plant communities between 600 and 2600 meters above sea level. In: Grace J, Ford ED, Jarvis PG (eds) Plants and Their Atmospheric Environments. Blackwell Scientific Publishers, Oxford, London, Edinburgh, pp 205–218

    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  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Kremers KS, Hollister RD, Oberbauer SF (2015) Diminished response of arctic plants to warming over time. PLoS One 10:e0116586

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar N, Kumar S, Ahuja PS (2004) Differences in the activation state of ribulose-1,5-bisphosphate carboxylase/oxygenase in barley, pea, and wheat at two altitudes. Photosynthetica 42:303–305

    Article  CAS  Google Scholar 

  • Kumar N, Kumar S, Ahuja PS (2005) Photosynthetic characteristics of Hordeum, Triticum, Rumex, and Trifolium species at contrasting altitudes. Photosynthetica 43:195–201

    Article  CAS  Google Scholar 

  • Lessard-Therrien M, Davies TJ, Bolmgren K (2014) A phylogenetic comparative study of flowering phenology along an elevational gradient in the Canadian subarctic. Int J Biometeorol 58:455–462

    Article  PubMed  Google Scholar 

  • Mächler F, Nösberger J (1978) The adaptation to temperature of photorespiration and of the photosynthetic carbon metabolism of altitudinal ecotypes of Trifolium repens L. Oecologia 35:267–276

    Article  PubMed  Google Scholar 

  • Manzaneda AJ, Rey PJ, Anderson JT, Raskin E, Weiss-Lehman C, Mitchell-Olds T (2015) Natural variation, differentiation, and genetic trade-offs of ecophysiological traits in response to water limitation in Brachypodium distachyon and its descendent allotetraploid B. hybridum (Poaceae). Evolution 69:2689–2704

    Article  PubMed  PubMed Central  Google Scholar 

  • Milbau A, Graae BJ, Shevtsova A, Nijs I (2009) Effects of a warmer climate on seed germination in the subarctic. Ann Bot 104:287–296

    Article  PubMed  PubMed Central  Google Scholar 

  • Nobel PS (1976) Photosynthetic rates of sun versus shade leaves of Hyptis emoryi Torr. Plant Physiol 58:218–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohsawa T, Ide Y (2008) Global patterns of genetic variation in plant species along vertical and horizontal gradients on mountains. Glob Ecol Biogeo 17:152–163

    Article  Google Scholar 

  • Pangtey YPS, Rawal RS, Bankoti NS, Samant SS (1990) Phenology of high-altitude plants of Kumaun in Central Himalaya, India. Int J Biometeorol 34:122–127

    Article  Google Scholar 

  • Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  PubMed  Google Scholar 

  • Peñuelas J, Filella I, Comas P (2002) Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. Glob Change Biol 8:531–544

    Article  Google Scholar 

  • Pinedo ML, Hernández GF, Conde RD, Tognetti JA (2000) Effect of low temperature on the protein metabolism of wheat leaves. Biol Plantarum 43:363–367

    Article  CAS  Google Scholar 

  • Pluess AR, Schutz W, Stöcklin J (2005) Seed weight increases with altitude in the Swiss Alps between related species but not among populations of individual species. Oecologia 144:55–61

    Article  PubMed  Google Scholar 

  • Polunin O, Stainton A (1984) Flowers of the Himalaya. Oxford University Press, Oxford, New York

    Google Scholar 

  • Premoli AC, Brewer CA (2007) Environmental vs. genetically driven variation in ecophysiological traits of Nothofagus pumilio from contrasting elevations. Aust J Bot 55:585–591

    Article  Google Scholar 

  • Qiang WY, Wang XL, Chen T, Feng HY, An LZ, He YQ, Wang G (2003) Variations of stomatal density and carbon isotope values of Picea crassifolia at different altitudes in the Qilian Mountains. Trees 17:258–262

    Google Scholar 

  • Rawat DS (2012) Flowering phenology on altitudinal gradient in the Himalaya. Curr Sci 103:1281–1284

    Google Scholar 

  • Saxe H, Cannell MGR, Johnsen O, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytol 149:369–400

    Article  CAS  Google Scholar 

  • Schoettle AW, Rochelle SG (2000) Morphological variation of Pinus flexilis (Pinaceae), a bird-dispersed pine, across a range of elevations. Am J Bot 87:1797–1806

    Article  CAS  PubMed  Google Scholar 

  • Simons AM, Johnston MO (2000) Variation in seed traits of Lobelia inflate (Campanulaceae): sources and fitness consequences. Am J Bot 87:124–132

    Article  CAS  PubMed  Google Scholar 

  • Slayback DA, Pinzon JE, Los SO, Tucker CJ (2003) Northern hemisphere photosynthetic trends 1982-99. Glob Change Biol 9:1–15

    Article  Google Scholar 

  • Soolanayakanahally RY, Guy RD, Silim SN, Drewes EC, Schroeder WR (2009) Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant Cell Environ 32:1821–1832

    Article  CAS  PubMed  Google Scholar 

  • Starr G, Oberbauer SF, Pop ERICW (2000) Effects of lengthened growing season and soil warming on the phenology and physiology of Polygonum bistorta. Glob Change Biol 6:357–369

    Article  Google Scholar 

  • Stinson KA (2004) Natural selection favors rapid reproductive phenology in Potentilla pulcherrima (Rosaceae) at opposite ends of a subalpine snowmelt gradient. Am J Bot 91:531–539

    Article  PubMed  Google Scholar 

  • Streb P, Shang W, Feierabend J, Bligny R (1998) Divergent strategies of photoprotection in high-mountain plants. Planta 207:313–324

    Article  CAS  Google Scholar 

  • Studer S, Appenzeller C, Defila C (2005) Inter-annual variability and decadal trends in Alpine spring phenology: a multivariate analysis approach. Clim Change 73:395–414

    Article  Google Scholar 

  • Todaria NP, Purohit AN (1979) Functional dynamics of plants at different altitudes. I. Growth pattern of Artemisia vulgaris. Indian J Pl Physiol 22:230–240

    Google Scholar 

  • Tranquillini W (1979) Tree existence at high altitudes with special reference to the European Alps. In: Physiological ecology of the alpine timberline (Ecological Studies), vol 31, p 137. Springer, Berlin, Heidelberg, New York

  • van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60

    Article  PubMed  Google Scholar 

  • Vats SK, Kumar S (2006) Photosynthetic response of Podophyllum hexandrum Royle from different altitudes in Himalayan ranges. Photosynthetica 44:136–139

    Article  Google Scholar 

  • Villemereuil P, de Gaggiotti OE, Mouterde M, Till-Bottraud I (2016) Common garden experiments in the genomic era: new perspectives and opportunities. Heredity 116:249–254

    Article  PubMed  Google Scholar 

  • Vitasse Y, Porte AJ, Kremer A, Michalet R, Delzon S (2009) Responses of canopy duration to temperature changes in four temperate tree species: relative contributions of spring and autumn leaf phenology. Oecologia 161:187–198

    Article  PubMed  Google Scholar 

  • Vitasse Y, Hoch G, Randin CF, Lenz A, Kollas C, Scheepens JF, Körner C (2013) Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species. Oecologia 171:663–678

    Article  PubMed  Google Scholar 

  • Voleníková M, Tichá I (2001) Insertion profiles in stomatal density and sizes in Nicotiana tabacum L. plantlets. Biol Plantarum 44:161–165

    Article  Google Scholar 

  • Weigh M, Karlsson PS (1999) Growth response of altitudinal ecotypes of mountain birch to temperature and fertilisation. Oecologia 119:16–23

    Article  Google Scholar 

  • Welp LR, Randerson JT, Liu HP (2007) The sensitivity of carbon fluxes to spring warming and summer drought depends on plant functional type in boreal forest ecosystems. Agric For Meteorol 147:172–185

    Article  Google Scholar 

  • Williams DG, Mack RN, Black RN (1995) Ecophysiology of introduced Pennisetum setaceum on Hawaii: the role of phenotypic plasticity. Ecology 76:1569–1580

    Article  Google Scholar 

  • Wirth LR, Graf R, Gugerli F, Landergott U, Holderegger R (2010) Between-year variation in seed weights across altitudes in the high-alpine plant Eritrichium nanum. Plant Ecol 207:227–231

    Article  Google Scholar 

  • Wise RR (1995) Chilling enhanced photooxidation: the production, action and study of reactive oxygen species produced during chilling in the light. Photosynth Res 45:79–97

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Ziello C, Estrella N, Kostova M, Koch E, Menzel A (2009) Influence of altitude on phenology of selected plant species in the Alpine region (1971–2000). Clim Res 39:227–234

    Article  Google Scholar 

Download references

Acknowledgements

Authors thank Council of Scientific and Industrial Research (CSIR) for funding through mission mode Project on “Plant diversity: studying adaptation biology and understanding/exploiting medicinally important plants for useful bioactives” (SIMPLE-BSC0109). RJ gratefully acknowledges the Junior/Senior Research Fellowship awarded by University Grants Commission (UGC). The manuscript represents IHBT communication number 3710.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Surender Kumar Vats.

Additional information

Communicated by U. Feller.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11738_2017_2396_MOESM1_ESM.jpg

Supplementary Fig. 1 Germination pattern of seeds of Rumex nepalensis collected from four different elevations: SP sub-tropical population (800 m amsl); STP sub-temperate population (1300 m amsl); TP temperate population (2200 m amsl); AP alpine population (4000 m amsl) and grown at 15 °C and 25 °C in growth chamber (JPEG 135 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jandrotia, R., Pal, P.K., Kumar, S. et al. Phenotypic variation between high and low elevation populations of Rumex nepalensis in the Himalayas is driven by genetic differentiation. Acta Physiol Plant 39, 99 (2017). https://doi.org/10.1007/s11738-017-2396-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-017-2396-7

Keywords

Navigation