Abstract
Elucidation of the structural and physiological adaptations developed against environmental determinants is a key to understand acclimation and capability to withstand cold in plants colonizing high altitudes. In the present study, two Sorghum species, S. arundinaceum and S. nitidum, were collected from three different elevations (800, 1800 and 2800 m a.s.l.) in the Neelum Valley, Azad Jammu and Kashmir. Above-ground biomass decreased but root growth increased along the altitude gradient in both species. The accumulation of ionic content in root and shoot was high in S. nitidum and low in S. arundinaceum. In S. nitidum, chlorophyll contents showed a significant increase from low to high altitude, while in S. arundinaceum, chlorophyll content decreased with increase in altitude. Both Sorghum species generally showed reduction in root epidermis thickness while metaxylem and phloem area increased along the altitude gradient. Stem and leaf area showed intensive sclerification and increased cortical cell area in S. nitidum, but sclerification in S. arundinaceum reduced from low to high altitude. Stomatal density and stomatal area were reduced in both Sorghum species from lower elevation to higher elevation. In S. arundinaceum, small angular prickles at the leaf margins were observed. It was concluded that narrow vessels, extensive sclerification and hairiness assisted both grasses to tolerate freezing-induced damage and their survival at extremely cold temperatures.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
(1) The voucher specimens used for plant identification are deposited to the herbarium facility of the Department of Botany, University of Agriculture, Faisalabad, and are available for verification on request. (2) Anatomical slides, photographs and raw data calculated from these photographs are available with primary author and can be requested if needed.
References
Ahmad KS, Hameed M, Fatima S, Ashraf M, Ahmad F, Naseer M, Akhtar N (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
Ahmad KS, Hameed M, Fatima S, Ashraf M, Ahmad F, Naseer M, Akhtar N (2016) 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
Alvarez JM, Rocha JF, Machado SR (2008) Bulliform cells in Loudetiopsis chrysothrix (Nees) Conert and Tristachya leiostachya Nees (Poaceae): structure in relation to function. Braz Arch Biol Technol 51:113–119. https://doi.org/10.1590/S1516-89132008000100014
Arnon DI (1949) Copper enzymes in isolated chloroplasts Polyphenoloxidase in Beta Vulgaris. Plant Physiol 24:1–10
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. https://doi.org/10.1093/aob/mcl068
Chaloner WG, Cope MJ (1982) Interaction of plant evolution, wildfire, atmospheric composition and climate. Third N Am Paleontol Convention Proc 1:83–85
Charan G, Bharti VK, Jadhav SE, Kumar S, Acharya S, Kumar P, Gogoi D, Srivastava RB (2013) Altitudinal variations in soil physico-chemical properties at cold desert high altitude. J Soil Sci Plant Nutr 13:267–277. https://doi.org/10.4067/S0718-95162013005000023
Dufour A, Gadallah F, Wagner HH, Guisan A, Buttler A (2006) Plant species richness and environmental heterogeneity in a mountain landscape: effects of variability and spatial configuration. Ecography 29:573–584. https://doi.org/10.1111/j.0906-7590.2006.04605.x
Ellen, KK (1988) Relationship of shattercane to cultivated and feral Sorghum in the Mid-Western United States. Retrospective Theses and Dissertations, Paper 8859. Submitted to Iowa State University, Ames, Iowa, USA, https://core.ac.uk/download/pdf/38899486.pdf
Fatima S, Hameed M, Ahmad F, Ashraf M, Ahmad R (2018) Structural and functional modifications in a typical arid zone species Aristida adscensionis L. along altitudinal gradient. Flora 249:172–182. https://doi.org/10.1016/j.flora.2018.11.003
Gonçalves JFDC, Marenco RA, Vieira G (2001) Concentration of photosynthetic pigments and chlorophyll fluorescence of mahogany and tonka bean under two light environments. Rev Bras Fisiol Veg 13:149–157. https://doi.org/10.1590/S0103-31312001000200004
Hacke UG, Spicer R, Schreiber SG, Plavcová L (2017) An ecophysiological and developmental perspective on variation in vessel diameter. Plant Cell Environ 40:831–845. https://doi.org/10.1111/pce.12777
Hameed MA, Ashraf MU, Naz N, Al-Qurainy F (2010) Anatomical adaptations of Cynodon dactylon (L.) Pers. from salt range Pakistan, to salinity stress. I. Root and stem anatomy. Pak J Bot 42:279–289
Hameed M, Nawaz T, Ashraf M, Naz N, Batool R, Ahmad MSA, Riaz A (2013) Physioanatomical adaptations in response to salt stress in Sporobolus arabicus (Poaceae) from the Salt Range, Pakistan. Turk J Bot 37:715–724. https://doi.org/10.3906/bot-1208-1
Hazrati S, Tahmasebi-Sarvestani Z, Modarres-Sanavy SA, Mokhtassi-Bidgoli A, Nicola S (2016) Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L. Plant Physiol Biochem 106:141–148. https://doi.org/10.1016/j.plaphy.2016.04.046
Horgan FG, Quiring DT, Lagnaoui A, Pelletier Y (2009) Effects of altitude of origin on trichome-mediated anti-herbivore resistance in wild Andean potatoes. Flora 204:49–62. https://doi.org/10.1016/j.flora.2008.01.008
Hubálek Z (1982) Coefficients of association and similarity, based on binary (presence-absence) data: an evaluation. Biol Rev 57:669–689
Jiang ZY, Li XY, Wei JQ, Chen HY, Li ZC, Liu L, Hu X (2018) Contrasting surface soil hydrology regulated by biological and physical soil crusts for patchy grass in the high-altitude alpine steppe ecosystem. Geoderma 326:201–209. https://doi.org/10.1016/j.geoderma.2018.04.009
Jin XM, Zhang YK, Schaepman ME, Clevers JG, Su Z, Cheng J, Jiang J, van Genderen J (2008) Impact of elevation and aspect on the spatial distribution of vegetation in the Qilian mountain area with remote sensing data. In: XXIth ISPRS Congress, Beijing, 3–11 July 2008, pp: 1385–1390
Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574. https://doi.org/10.1016/j.tree.2007.09.006
Kosmala A, Bocian A, Rapacz M, Jurczyk B, Zwierzykowski Z (2009) Identification of leaf proteins differentially accumulated during cold acclimation between Festuca pratensis plants with distinct levels of frost tolerance. J Exp Bot 60:3595–3609. https://doi.org/10.1093/jxb/erp205
Královec J, Pocová L, Jonášová M, Macek P, Prach K (2009) Spontaneous recovery of an intensively used grassland after cessation of fertilizing. Appl Veg Sci 12:391–397. https://doi.org/10.1111/j.1654-109X.2009.01032.x
Liu W, Zheng L, Qi D (2020) Variation in leaf traits at different altitudes reflects the adaptive strategy of plants to environmental changes. Ecol Evol 10:8166–8175. https://doi.org/10.1002/ece3.6519
Ludwig JA, Reynolds JF (1988) Statistical ecology: a primer in methods and computing, vol 1. John Wiley & Sons, Hoboken
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. Arctic Antarctic Alp Res 44:62–66. https://doi.org/10.1657/1938-4246-44.1.62
Malik ZA, Nautiyal MC (2016) Species richness and diversity along the altitudinal gradient in Tungnath, the Himalayan benchmark site of HIMADRI. Trop Plant Res 3:396–407
Malik ZA, Hussain A, Iqbal K, Bhatt AB (2014) Species richness and diversity along the disturbance gradient in Kedarnath wildlife sanctuary and its adjoining areas in Garhwal Himalaya, India. Int J Curr Res 6:10918–10926
Maulana F, Tesso TT (2013) Cold temperature episode at seedling and flowering stages reduces growth and yield components in Sorghum. Crop Sci 53:564–574. https://doi.org/10.2135/cropsci2011.12.0649
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/S1360-1385(02)02312-9
Monteiro MV, BlanušaT VA, Hadley P, Cameron RW (2016) Relative importance of transpiration rate and leaf morphological traits for the regulation of leaf temperature. Aust J Bot 64:32–44. https://doi.org/10.1071/BT15198
Nautiyal MC, Nautiyal BP, Prakash V (2004) Effect of grazing and climatic changes on alpine vegetation of Tungnath, Garhwal Himalaya, India. Environmentalist 24:125–134
Pausas JG, Austin MP (2001) Patterns of plant species richness in relation to different environments: an appraisal. J Veg Sci 12:153–166. https://doi.org/10.2307/3236601
Peng Y, Yang Z, Zhang H, Cui C, Qi X, Luo X, Tao X, Wu T, Chen H, Shi H, Su B (2011) Genetic variations in Tibetan populations and high-altitude adaptation at the Himalayas. Mol Biol Evol 28:1075–1081. https://doi.org/10.1093/molbev/msq290
Poorter L, Rozendaal DM (2008) Leaf size and leaf display of thirty-eight tropical tree species. Oecologia 158:35–46. https://doi.org/10.1007/s00442-008-1131-x
Reinoso H, Sosa L, Ramírez L, Luna V (2004) Salt-induced changes in the vegetative anatomy of Prosopis strombulifera (Leguminosae). Can J Bot 82:618–628. https://doi.org/10.1139/b04-040
Salick J, Zhendong F, Byg A (2009) Eastern Himalayan alpine plant ecology, Tibetan ethnobotany, and climate change. Global Environ Chang 19:147–155. https://doi.org/10.1016/j.gloenvcha.2009.01.008
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. https://doi.org/10.1046/j.1365-313x.2001.01052.x
Shinwari ZK, Qaisar M (2011) Efforts on conservation and sustainable use of medicinal plants of Pakistan. Pak J Bot 43:5–10
Steel RGD, Torrie JH (1986) Principles and procedures of statistics: a biometrical approach. McGraw-Hill, NY
Taguchi Y, Wada N (2001) Variations of leaf traits of an alpine shrub Sieversia pentapetala along an altitudinal gradient and under a simulated environmental change. Polar Biosci 14:79–87
Tasser E, Tappeiner U (2002) Impact of land use changes on mountain vegetation. Appl Veg Sci 5:173–184. https://doi.org/10.1111/j.1654-109X.2002.tb00547.x
Thomashow MF (1999) Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599. https://doi.org/10.1146/annurev.arplant.50.1.571
Tikhonov G, Abrego N, Ovaskainen DD, O, (2017) Using joint species distribution models for evaluating how species-to-species associations depend on the environmental context. Methods Ecol Evol 8:443–452. https://doi.org/10.1111/2041-210X.12723
Titshall LW, Connor TGO, Morris CD (2000) Effect of long-term exclusion of fire and herbivory on the soils and vegetation of sour grassland. Afr J Range Forage Sci 17:70–80. https://doi.org/10.2989/10220110009485742
Vasellati V, Oesterheld M, Medan D, Loreti J (2001) Effects of flooding and drought on the anatomy of Paspalum dilatatum. Ann Bot 88:355–360. https://doi.org/10.1006/anbo.2001.1469
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38
Yoshida S, Forno DA, Cock JH (1971) Laboratory manual for physiological studies of rice. IRRI, Los Banos
Acknowledgements
This manuscript has been derived from Ph.D. thesis of the first author submitted to University of Agriculture, Faisalabad.
Funding
This research work is a result of independent studies and there is no involvement of any individual or institutional funding agency.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that there is no conflict of interest with any individual, and educational, industrial or commercial institution.
Ethical approval
The study does not include any animal or human subjects and no specific ethical approval is needed. Other necessary guidelines set by University of Agriculture, Faisalabad for handling of plant material during conduction of laboratory work were followed. All samplings were done with the least possible disturbances to plant communities and environment. After completion of study, all experimental materials were properly discarded/incinerated in a controlled environment to avoid bio-contamination.
Publication Ethic statements
It is certified that the manuscript is the product of an original study and is submitted solely to this Journal for consideration. It is not submitted to any other Journal, in part or full, for simultaneous consideration nor has been previously published in any form or language (other than as a thesis of the first author, which is properly acknowledged). There is no plagiarism/self-plagiarism, salami-slicing/publishing, secondary publication nor near verbatim. All data presented in this manuscript is product of our own study and the manuscript does not contain any copyrighted material (data tables or figures). All results and data are presented clearly, honestly, and without fabrication, falsification or inappropriate data manipulation (including image-based manipulation).
Consent to participate
The contribution of all participants/parties involved in this study have been appreciated either in authorship OR acknowledged in the acknowledgement section. All contributors listed in this manuscript have substantially participated in this study and preparation of the manuscript.
Consent for publication
All authors agree to publish and there is no conflict for publication of this manuscript for publication in this Journal.
Additional information
Communicated by B. Zheng.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ahmad, K.S., Javaid, A., Hameed, M. et al. Survival strategies in two high altitude Sorghum species from western Himalayas. Acta Physiol Plant 44, 60 (2022). https://doi.org/10.1007/s11738-022-03392-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-022-03392-9