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Beating cold by being tough: impact of elevation on leaf characteristics in Phleum himalaicum Mez. endemic to Himalaya

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Abstract

Effect of altitude on leaf responses in Phleum himalaicum populations was evaluated at three different elevation levels, viz. (Low 1200 m.a.s.l.), middle (1600 m a.s.l.) and high (1900 m a.s.l.) in western part of Himalaya. We hypothesized that physico-chemical properties of soil varied along elevation and Phleum populations located at high elevation would adapt more distinct morphological and physiological traits than those originating from middle and low elevation sites. Our study revealed that soil pH, Ec Mg, Ca, and P decreased at high elevation however, significant increase was recorded in soil K, organic matter, and total nitrogen along the elevation gradient. A significant correlation between leaf characteristics and elevation sites was recorded along the gradient. The outcomes of this study showed that highland population had better adjustments under low temperature and exhibited adaptive traits. These were, decreased number of leaves and leaf area, increased leaf blade thickness, intensive sclerification, and greater stomatal and trichome density. Apart from these, high elevation population had more physiological adjustment in terms of low stomatal conductance, low transpiration rate, high water use efficiency, and synthesis of more osmolytes in leaf. We argued that certain level of sugar and protein must be attained by high population to dodge the aggressive climatic forces in order to grow successfully at the highest elevation. Furthermore, altitude between 1600 and 1900 m was more likely an optimum zone for vigorous growth of P. himalaicum at the highest level of elevation.

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References

  • Ahmad KS, Qureshi R, Hameed M, Ahmad F, Nawaz T (2012) Conservation assessment and medicinal importance of some plants resources from Sharda, Neelum Valley, Azad Jammu and Kashmir, Pakistan. Int J Agric Biol 14:997–1000

    Google Scholar 

  • Ahmad KS, Hameed M, Fatima S, Ashraf M, Ahmad F, Naseer M, Akhtar N (2016a) Morpho-anatomical and physiological adaptations to high elevation in some Aveneae grasses from Neelum Valley, Western Himalayan Kashmir. Acta Physiol Plant 38:93. https://doi.org/10.1007/s11738-016-2114-x

    Article  Google Scholar 

  • Ahmad KS, Hameed M, Ahmad F, Sadia B (2016b) Edaphic factors as major determinants of plant distribution of temperate Himalayan grasses. Pak J Bot 48:567–573

    CAS  Google Scholar 

  • Ahmad KS, Hameed M, Jiabin D, Ashraf M, Hamid A, Ahmad F, Fatima S, Akhtar N (2016c) Ecotypic adaptations in Bermuda grass (Cynodon dactylon) for altitudinal stress tolerance. Biologia 71:885–8895

    Article  CAS  Google Scholar 

  • Ahmad KS, Hamid A, Nawaz F, Hameed M, Ahmad F, Deng J, Akhtar N, Wazarat A, Mahroof S (2017) Ethnopharmacological studies of indigenous plants in Kel village, Neelum Valley, Azad Kashmir, Pakistan. J Ethnobiol Ethnomed 13:68. https://doi.org/10.1186/s13002-017-0196-1

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atkin OK, Botman B, Lambers H (1996) The causes of inherently slow growth in alpine plants: an analysis based on the underlying carbon economies of alpine and lowland Poa species. Funct Ecol 10:698–707

    Article  Google Scholar 

  • Bai YJ, Chen LQ, Ranhotra PS, Wang Q, Wang YF, Li CS (2015) Reconstructing atmospheric CO2 during the Plio–Pleistocene transition by fossil Typha. Glob Change Biol 21:874–881

    Article  Google Scholar 

  • Ball MC, Canny MJ, Huang CX, Heady RD (2004) Structural changes in acclimated and unacclimated leaves during freezing and thawing. Funct Plant Biol 31:29–40

    Article  Google Scholar 

  • Balsamo RA, Willigen CV, Bauer AM, Farrant J (2006) Drought tolerance of selected Eragrostis species correlates with leaf tensile properties. Ann Bot 97:985–991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bano S, Rehman A, Winiger M (2009) Altitudinal variation in the content of protein, proline, sugar and abscisic acid (ABA) in the alpine herbs from Hunza Valley, Pakistan. Pak J Bot 41:1593–1602

    Google Scholar 

  • Beniston M (2003) Climatic change in mountain regions: a review of possible impacts. Clim Change 59:5–31

    Article  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    Article  CAS  Google Scholar 

  • Clayton WD, Harman KT Williamson H (2006) World Grass Species—Synonymy database. The Board of Trustees of the Royal Botanic Gardens, Kew

  • Cohen SS, Gale J, Poljakoff-Mayber A, Shmida A, Suraqui S (1981) Transpiration and the radiation climate of the leaf on Mt. Hermon: a Mediterranean mountain. J Ecol 69:391–403

    Article  Google Scholar 

  • Cook D, Fowler S, Fiehn O, Tomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243–15248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cope TA (1982) Flora of Pakistan, vol 143. Department of Botany, University of Karachi, Karachi, pp 1–678

    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 

  • De Frenne P, Graae BJ, Rodriguez-Sanchez F, Kolb A, Chabrerie O, Decocq G, De Kort H, Diekmann M, Eriksson O (2013) Latitudinal gradients as natural laboratories to infer species responses to temperature. J Ecol 101:784–795

    Article  Google Scholar 

  • Devi BSR, Kim YJ, Selvi SK, Gayathri S, Altanzul K, Parvin S, Yang DU, Lee OR, Lee S, Yang DC (2012) Influence of potassium nitrate on antioxidant level and secondary metabolite genes under cold stress in Panax ginseng. Russ J Plant Physiol 59:318–325

    Article  CAS  Google Scholar 

  • Dierig DA, Adama NR, Mackey BE, Dahlquist GH, Coffelt TA (2006) Temperature and elevation effects on plant growth, development, and seed production of two Lesquerella species Indus Crops. Prod 24:17–25

    Google Scholar 

  • Falster DS, Westoby M (2005) Alternative height strategies among 45 dicot rain forest species from tropical Queensland. Aust J Ecol 93:521–535

    Article  Google Scholar 

  • Fatemeh Z, Tajik S, Soleimanpour S (2011) Effects of elevation on anatomy and concentration of Crocin, Picrocrocin and Safranal in Crocus sativus L. Aust J Crop Sci 5:831–838

    Google Scholar 

  • Feng Q, Centritto M, Cheng R, Liu S, Shi Z (2013) Leaf functional trait responses of Quercus aquifolioides to high elevations. Int J Agric Biol 15:69–75

    CAS  Google Scholar 

  • Gale J (1973) Experimental evidence for the effect of barometric pressure on photosynthesis and transpiration. Ecol Conserv (UNESCO) 5:289–293

    Google Scholar 

  • Gale J (2004) Plant and altitude-revisited. Ann Bot 2:199

    Article  Google Scholar 

  • Griffiths RP, Madritch MD, Swanson AK (2009) The effects of topography on forest soil characteristics in the Oregon Cascade Mountains (USA): implications for the effects of climate change on soil properties. For Ecol Manag 257:1–7

    Article  Google Scholar 

  • Guerin GR, Wen H, Lowe AJ (2012) Leaf morphology shift linked to climate change. Biol Lett 8:882–886

    Article  PubMed  PubMed Central  Google Scholar 

  • Gupta SM, Grover A, Ahmed Z (2012) Identification of abiotic stress responsive genes from Indian high elevation Lepidium latifolium L. Def Sci J 62:315–318

    Article  CAS  Google Scholar 

  • Hammond KA, Roth J, Janes DN, Dohm MR (1999) Morphological and physiological responses to altitude in deer mice Peromyscus maniculatus. Physiol Biochem Zool 72:613–622

    Article  CAS  PubMed  Google Scholar 

  • Herrick GT, Friedland AJ (1991) Winter desiccation and injury of subalpine red spruce. Tree Physiol 8:23–36

    Article  CAS  PubMed  Google Scholar 

  • Hovenden MJ, Schoor JKV (2006) The response of leaf morphology to irradiance depends on elevation of origin in Nothofagus cunninghamii. New Phytol 169:291–297

    Article  PubMed  Google Scholar 

  • Hovenden MJ, Vander Schoor JK (2004) Nature versus nurture in the leaf morphology of Southern beech, Nothofagus cunninghamii (Nothofagaceae). New Phytol 161:585–594

    Article  Google Scholar 

  • Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Kellar WA, Selvaraj G (2000) Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol 122:747–756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    Article  Google Scholar 

  • Ivanov AG, Sane PV, Zeinalov Y, Malmberg G, Gardeström P, Huner NPA, Öquist G (2001) Photosynthetic electron transport adjustments in overwintering Scots pine (Pinus sylvestris L.). Planta 213:575–585

    Article  CAS  PubMed  Google Scholar 

  • Jan G, Kahan M, Ahmad M, Iqbal Z, Afzal A, Afzal M, Shah GM, Majid A, Fiaz M, Zafar M, Waheed A, Gul F (2011) Nutritional analysis, micronutrients and chlorophyll contents of Cichorium intybus L. J Med Plants Res 5:2452–2456

    CAS  Google Scholar 

  • Jump AS, Penuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8:1010–1020

    Article  Google Scholar 

  • Kandwal MK, Gupta BK (2009) An update on grass flora of Uttarkhand. Indian J For 32:657–668

    Google Scholar 

  • Kessler M (2001) Patterns of diversity and range size of selected plant groups along an elevational transect in the Bolivian Andes. Biodivers Conserv 10:1897–1921

    Article  Google Scholar 

  • Kidanemariam A, Gebrekidan H, Mamo Kibret K (2012) Impact of altitude and land use type on some physical and chemical properties of acidic soils in Tsegede Highlands, Northern Ethiopia. Open J Soil Sci 2:223–233

    Article  CAS  Google Scholar 

  • Klein T, Di Matteo G, Rotenberg E, Cohen S, Yakir D (2013) Differential ecophysiological response of a major Mediterranean pine species across a climatic gradient. Tree Physiol 33:26–36

    Article  PubMed  Google Scholar 

  • Kofidis G, Bosabalidis AM, Moustakas M (2003) Contemporary seasonal and altitudinal variations of leaf structural features in Oregano (Origanum vulgare L.). Ann Bot 92:635–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kofidis G, Bosabalidis AM, Moustakas M (2007) Combined effect of elevation and season on leaf characteristics of Chenopodium vulgare L. (Labiatae). Environ Exp Bot 60:69–76

    Article  Google Scholar 

  • Köhler L, Gieger T, Leuschner C (2006) Altitudinal change in soil and foliar nutrient concentrations and in microclimate across the tree line on the subtropical island mountain Mt. Teide (Canary Islands). Flora 201:202–214

    Article  Google Scholar 

  • Koppel A, Heinsoo K (1994) Variability in cuticular resistance of Picea abies (L.) Karst. and its significance in winter desiccation. Proc Estonian Acad Sci 4:56–63

    Google Scholar 

  • Körner C (2007) The use of elevation in ecological research. Trends Ecol Evol 22:569–574

    Article  PubMed  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, Menendez-Riedl S, Smeets-Scheel A (1989) Functional morphology of mountain plants. Flora 182:353–383

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kumar N, Vats KS, Kumar S, Ahuja PS (2008) Altitude-related changes in activities of carbon metabolism enzymes in Rumex nepalensis. Photosynthetica 46(4):611–614

    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 

  • Larcher W (1985) Winter stress in high mountains. In: Turner H, Tranquillini W (eds) Establishment and tending of subalpine forest: research and management. Eidgenössische Anstalt für forstliches Versuchswe-sen, Birmensdorf, pp 11–19

    Google Scholar 

  • Li GY, Yang DM, Sun SC (2008a) Allometric relationships between lamina area, lamina mass, and petiole mass of 93 temperate woody species vary with leaf habit, leaf form, and altitude. Funct Ecol 22:557–564

    Article  Google Scholar 

  • Li H, Qiang S, Qian Y (2008b) Physiological response of different croftonwood (Eupatorium adenophorum) population to low temperature. Weed Sci 56:196–202

    Article  CAS  Google Scholar 

  • Li Z, Ji C, Liu J (2008c) Leaf area calculating based on digital image. In: Li D (ed) Computer And computing technologies in agriculture, vol II. CCTA 2007. The International Federation for Information Processing, vol 259. Springer, Boston

    Google Scholar 

  • Liu L, Xu SM, Woo KC (2005) Solar UV-B radiation on growth, photosynthesis and the xanthophylls cycle in tropical Acacia and Eucalyptus. Environ Exp Bot 54:121–130

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL Randall RJ (1951) Protein Measurement with the Folin Phenol Reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Macek P, Mackova J, de Bello F (2009) Morphological and ecophysiological traits sha** altitudinal distribution of three Polylepis treeline species in the dry tropical Andes. Acta Oecol 35:778–785

    Article  Google Scholar 

  • Macek P, Leoš K, Lubomir A, Jiři D, Zuzana C, Francesco B, Miroslav D, Klára Ř (2012) Plant nutrient content does not simply increase with elevation under the extreme environmental conditions of Ladakh, NW Himalaya. Antarct Alp Res 44:62–66

    Article  Google Scholar 

  • Malgorzata B, Nevena S, Zaltko Z, Daniela G (2008) Physiological response of some genotypes (Lycopersicum esculentum L.) to high temperature stress. J Cent Eur Agric 9:723–732

    Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Moles AT, Leishman MR (2008) The seedling as part of a plant’s life history strategy. In: Leck MA, Parker VT, Simpson RL (eds) Seedling ecology and evolution. Cambridge University Press, Cambridge, pp 217–238

    Chapter  Google Scholar 

  • Moor S, Stein WH (1948) Photometric ninhydrin method for use in the chromatography of amino acids. J Biol Chem 176:367–388

    Google Scholar 

  • Morecroft MD, Woodward FI (1996) Experiments on the causes of altitudinal differences in the leaf nutrient contents, size and δ13C of Alchemilla alpine. New Phytol 134:471–479

    Article  CAS  Google Scholar 

  • Pato J, Obeso JR (2012) Growth and reproductive performance in bilberry (Vaccinium myrtillus) along an elevation gradient. Ecoscience 19:59–68

    Article  Google Scholar 

  • Peng YH, Zhu YF, Mao YQ (2004) Alkali grass resists salt stress through high K and an endodermis barrier to Na. J Exp Bot 55:939–949

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Rajashekar CB, Burke MJ (1996) Freezing characteristics of rigid plant tissues. Development of cell tension during extracellular freezing. Plant Physiol 111:597–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rajashekar CB, Lafta A (1996) Cell-wall changes and cell tension in response to cold acclimation and exogenous abscisic acid in leaves and cell cultures. Plant Physiol 111:605–612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rekarte-Cowie I, Ebshish OS, Mohamed KS, Pearce RS (2008) Sucrose helps regulate cold acclimation of Arabidopsis thaliana. J Exp Bot 59:4205–4217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sangwan V, Foulds I, Singh J, Dhindsa RS (2001) Cold activation of Brassica napus BN115 promter is mediated by structural changes in membranes and cytoskeleton and requires Ca2+ influx. Plant J 27:1–12

    Article  CAS  PubMed  Google Scholar 

  • Sariyildiz T, Anderson JM, Kucku M (2005) Effects of tree species and topography on soil chemistry, litter quality and decomposition in Northeast Turkey. Soil Biol Biochem 37:1695–1706

    Article  CAS  Google Scholar 

  • Scholz FG, Bucci SJ, Arias N, Meinzer FC, Goldstein G (2012) Osmotic and elastic adjustments in cold desert shrubs differing in rooting depth: co** with drought and subzero temperatures. Oecologia 170:885–897

    Article  PubMed  Google Scholar 

  • Schreiber L, Hartmann K, Skrabs M (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280

    CAS  Google Scholar 

  • Scrase-Field SA, Knight MR (2003) Calcium: just a chemical switch? Curr Opin Plant Biol 6:500–506

    Article  CAS  PubMed  Google Scholar 

  • Shi Z, Haworth M, Feng Q, Cheng R, Centritto M (2015) Growth habit and leaf economics determine gas exchange responses to high elevation in an evergreen tree, a deciduous shrub and a herbaceous annual. AoB Plants 7:plv115. https://doi.org/10.1093/aobpla/plv115

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Solecka D, Żebrowski J, Kacperska A (2008) Are pectins involved in cold acclimation and de-acclimation of winter oil-seed rape plants? Ann Bot 101:521–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stefanowska M, Kuraś M, Kubacka-Zebalska M, Kacperska A (1999) Low temperature affects pattern of leaf growth and structure of cell walls in winter oilseed rape (Brassica napus L., var. oleifera L.). Ann Bot 84:313–319

    Article  Google Scholar 

  • Sundqvist MK, Sanders NJ, Wardle DA (2013) Community and ecosystem responses to elevational gradients: processes, mechanisms, and insights for global change. Annu Rev Ecol Evol Syst 44:261–280

    Article  Google Scholar 

  • Suzuki S (1998) Leaf phenology, seasonal changes in leaf quality and herbivory pattern of Sanguisorba tenuifolia at different altitudes. Oecologia 117:169–176

    Article  PubMed  Google Scholar 

  • Taguchi Y, Wada N (2001) Variations of leaf traits of an alpine shrub Sieversia pentapetala along an altitudinal gradient and under a stimulated environmental change. Polar Biosci 14:79–87

    Google Scholar 

  • Taji T, Ohsumi C, Luchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426

    Article  CAS  PubMed  Google Scholar 

  • Taub D (2010) Effects of rising atmospheric concentrations of carbon dioxide on plants. Nat Educ Knowl 3:21

    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 

  • Unal BT, Guvensen A, Dereboylu AE, Ozturk M (2013) Variations in the proline and total protein contents in Origanum sipyleum L. from different altitudes in Spil Mountain, Turkey. Pak J Bot 45:571–576

    Google Scholar 

  • Valladares F, Balaguer L, Martínez-Ferri E, Perez-Corona E, Manrique E (2002) Plasticity, instability and canalization: is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems? New Phytol 156:457–467

    Article  Google Scholar 

  • Venema JH, Eekhof M, Van Hasselt PR (2000a) Analysis of low-temperature tolerance of a tomato (Lycopersicon esculentum) cybrid with chloroplasts from a more chilling-tolerant L. hirsutum accession. Ann Bot 85:799–807

    Article  Google Scholar 

  • Venema JH, Villerius L, Van Hasselt PR (2000b) Effect of acclimation to suboptimal temperature on chilling-induced photodamage: comparison between a domestic and a high-elevation wild Lycopersicum species. Plant Sci 152:153–163

    Article  CAS  Google Scholar 

  • Vincent AG, Sundqvist MK, Wardle DA, Giesler R, Wang X (2014) Bioavailable soil phosphorus decreases with increasing elevation in a subarctic tundra landscape. PLoS ONE 9(3):e92942

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Walkley A, Black IA (1934) An examination of Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–37

    Article  CAS  Google Scholar 

  • Wang G, Feng X (2012) Response of plants’ water use efficiency to increasing atmospheric CO2 concentration. Environ Sci Technol 46(16):8610–8620. https://doi.org/10.1021/es301323m

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Weiser RL, Wallner SJ, Waddell JW (1990) Cell wall and extensin mRNA changes during cold acclimation of pea seedlings. Plant Physiol 93:1021–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolf B (1982) A comprehensive system of leaf analysis and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 13:1035–1059

    Article  CAS  Google Scholar 

  • Woodward FI (1979) The differential temperature responses of the growth of certain plant species from different elevations. II. Analyses of the control and morphology of leaf extension and specific leaf area of Phleum bertolonii D.C. and P. alpinum L. New Phytol 82:397–405

    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 

  • Xu JM, Tang C, Chen ZL (2006) The role of plant residues in pH change of acid soils differing in initial pH. Soil Biol Biochem 38:709–719

    Article  CAS  Google Scholar 

  • Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57(3):508–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young KR, Ulloa UC, Luteyn JL, Knapp S (2002) Plant evolution and endemism in Andean South America: an introduction. Bot Rev 68:4–27

    Article  Google Scholar 

  • Yu**g Z, Yong Z (2000) Studies on ultrastructure of Puccinellia tenuiflora under different salinity stress. Grassl China 4:30–32

    Google Scholar 

  • Zhang SB, Guan ZJ, Sun M, Zhang JJ, Cao KF et al (2012) Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae. Plos One 7(6):e40080. https://doi.org/10.1371/journal.pone0040080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao X, Tan H, Chen G (2016) Effect of organic osmolytes and ABA accumulated in twelve dominant desert plants of the Tengger Desert, China. Res Rev J Bot Sci 5:45–50

    Google Scholar 

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The project is not funded by any organization. We are thankful to editor of the Acta Physiologiae Plantarum and anonymous reviewers who spare their precious time to make our work more comprehensive and valuable.

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Ahmad, K.S., Hameed, M., Hamid, A. et al. Beating cold by being tough: impact of elevation on leaf characteristics in Phleum himalaicum Mez. endemic to Himalaya. Acta Physiol Plant 40, 56 (2018). https://doi.org/10.1007/s11738-018-2637-4

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