Abstract
Plants overcome environmental stress by generating metabolic pathways. Thus, it is crucial to understand the physiological mechanisms of plant responses to changing environments. Ardisia crenata var. bicolor has an important ornamental and medicinal value. To reveal the impact of elevational gradient on the habitat soil and plant physiological attributes of this species, we collected root topsoil (0–20 cm) and subsoil (20–40 cm) samples and upper leaves at the initial blooming phase, in a survey of six elevations at 1,257 m, 1,538 m, 1,744 m, 1,970 m, 2,135 m, and 2,376 m, with 18 block plots, and 5 sampling points at each site. Temperature decreases with an increase in elevation, and soil variables, and enzymatic activities fluctuated in both the topsoil and subsoil, with all of them increasing with elevation and decreasing with soil depth. Redundancy analysis was conducted to explore the correlation between the distribution of A. crenata var. bicolor along the elevational gradient and soil nutrients and enzyme activities, the soil properties were mainly affected by pH at low elevations, and governed by total phosphorus (TP) and available nitrogen (AN) at high elevations. The levels of chlorophyll, carbohydrates, and enzymatic activity except for anthocyanin in this species showed significant variation depending on physiological attributes evaluated at the different collection elevations. The decline in chlorophyll a and b may be associated with the adaptive response to avoid environmental stress, while its higher soluble sugar and protein contents play important roles in escaping adverse climatic conditions, and the increases in activities of antioxidant enzymes except peroxidase (POD) reflect this species’ higher capacity for reactive oxygen scavenging (ROS) at high elevations. This study provides supporting evidence that elevation significantly affects the physiological attributes of A. crenata var. bicolor on Gaoligong Mountain, which is helpful for understanding plant adaptation strategies and the plasticity of plant physiological traits along the elevational gradients.
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References
Ahmad KS, Hameed M, Deng J, et al. (2016) Ecotypic adaptations in Bermuda grass (Cynodon dactylon) for altitudinal stress tolerance. Biologia 71: 885–895. https://doi.org/10.1515/biolog-2016-0113
Ahmad KS, Javaid A, Hameed M, et al. (2022) Survival strategies in two high altitude Sorghum species from western Himalayas. Acta Physiol Plant 44. https://doi.org/10.1007/S11738-022-03392-9
Anderson JT, Willis JH, Mitchell-Olds T (2011) Evolutionary genetics of plant adaptation. Trends Genet 27: 258–266. https://doi.org/10.1016/j.tig.2011.04.001
Bao SD (2000) Soil Agricultural Chemistry Analysis. Beijing: Agricultural Press. (In Chinese).
Barnes PW, Ryel RJ, Flint SD (2017) UV screening in native and non-native plant species in the tropical alpine: implications for climate change-driven migration of species to higher elevations. Front Plant Sci 8: 1451. https://doi.org/10.3389/fpls.2017.01451
Basu PS, Berger JD, Turner NC, et al. (2007) Osmotic adjustment of Chickpea (Cicer arietinum) is not associated with changes in carbohydrate composition or leaf gas exchange under drought. Ann Appl Biol 150: 217–225. https://doi.org/10.1111/j.1744-7348.2007.00119.x
Bo F, Zhang Y, Chen HYH, et al. (2020) The C:N:P Stoichiometry of Planted and Natural Larix principis-rupprechtii Stands along Altitudinal Gradients on the Loess Plateau, China. Forests 11: 363. https://doi.org/10.3390/f11040363.
Byars SG, Papst W, Hoffmann AA (2007) Local adaptation and cogradient selection in the alpine plant, poa hiemata, along a narrow altitudinal gradient. Evolution 61: 2925–2941. https://doi.org/10.1111/j.1558-5646.2007.00248.x
Cenini VL, Fornara DA, McMullan G, et al. (2016) Linkages between extracellular enzyme activities and the carbon and nitrogen content of grassland soils. Soil Biol Biochem 96: 198–206. https://doi.org/10.1016/j.soilbio.2016.02.015
Chen B, Zhang X, Tao J, et al. (2014) The impact of climate change and anthropogenic activities on alpine grassland over the Qinghai-Tibet Plateau. Agr Forest Meteorol 189/190: 11–18. https://doi.org/10.1016/j.agrformet.2014.01.002
Chen R, Han C, Liu J, et al. (2018) Maximum precipitation altitude on the northern flank of the Qilian Mountains, northwest China. Hydrol Res 49: 1696–1710. https://doi.org/10.2166/nh.2018.121
Cui G, Li B, He W, et al. (2018) Physiological analysis of the effect of altitudinal gradients on Leymus secalinus on the Qinghai-Tibetan Plateau. PloS one 13: e0202881. https://doi.org/10.1371/journal.pone.0202881
Cui G, Wei X, Degen AA, et al. (2016) Trolox-equivalent antioxidant capacity and composition of five alpine plant species growing at different elevations on the Qinghai-Tibetan Plateau. Plant Ecol Divers 9: 387–396. https://doi.org/10.1080/17550874.2016.1261952
Du B, Kang H, Pumpanen J, et al. (2014) Soil organic carbon stock and chemical composition along an altitude gradient in the Lushan Mountain, subtropical China. Ecol Res 29: 433–439. https://doi.org/10.1007/s11284-014-1135-4
Dungait JAJ, Hopkins DW, Gregory AS, et al. (2012) Soil organic matter turnover is governed by accessibility not recalcitrance. Global Change Biol 18: 1781–1796. https://doi.org/10.1111/j.1365-2486.2012.02665.x
Edward A, Heidi S, Sarah B, et al. (2009) Tree species traits influence soil physical, chemical, and biological properties in high elevation forests. PloS one 4: e5964. https://doi.org/10.1371/journal.pone.0005964
Frenne P, Graae BJ, Rodríguez-Sánchez F, et al. (2013) Latitudinal gradients as natural laboratories to infer species’ responses to temperature (SOM). J Ecol 101: 784–795 https://doi.org/10.1111/1365-2745.12074
Gao L, Gou X, Deng Y, et al. (2017) Assessing the influences of tree species, elevation and climate on tree-ring growth in the Qilian Mountains of northwest China. Trees 31: 393–404 https://doi.org/10.1007/s00468-015-1294-0
Gebrehiwot K, Desalegn T, Woldu Z, et al. (2018) Soil organic carbon stock in Abune Yosef afroalpine and sub-afroalpine vegetation, northern Ethiopia. Ecol Process 7: 1–9. https://doi.org/10.1186/s13717-018-0117-9
Gilliam FS, Galloway JE, Sarmiento JS (2015) Variation with slope aspect in effects of temperature on nitrogen mineralization and nitrification in mineral soil of mixed hardwood forests. Can J Forest Res 45: 958–962. https://doi.org/10.1139/cjfr-2015-0087
Gratani L, Catoni R, Pirone G, et al. (2012) Physiological and morphological leaf trait variations in two Apennine plant species in response to different altitudes. Photosynthetica: International Journal for Photosynthesis Research 50: 15–23. https://doi.org/10.1007/s11099-012-0006-x
Hasanuzzaman M, Nahar K, Alam M, et al. (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14: 9643–9684. https://doi.org/10.3390/ijms14059643
Hazrati S, Tahmasebi-Sarvestani Z, Modarres-Sanavy SAM, et al. (2016) Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L. Plant Physiol Bioch 106: 141–148. https://doi.org/10.1016/j.plaphy.2016.04.046
He X, Hou E, Liu Y, et al. (2016) Altitudinal patterns and controls of plant and soil nutrient concentrations and stoichiometry in subtropical China. Sci Rep-UK 6. https://doi.org/10.1038/srep24261
Herold N, Schöning I, Gutknecht J, et al. (2014) Soil property and management effects on grassland microbial communities across a latitudinal gradient in Germany. Appl Soil Ecol 73: 41–50. https://doi.org/10.1016/j.apsoil.2013.07.009
Hossain MA, Pavel MAA, Harada K, et al. (2019) Tree species diversity in relation to environmental variables and disturbance gradients in a northeastern forest in Bangladesh. J Forestry Res 30: 2143–2150. https://doi.org/10.1007/s11629-015-3501-2
Huang B, DaCosta M, Jiang Y (2014) Research advances in mechanisms of turfgrass tolerance to abiotic stresses: from physiology to molecular biology. Crit Rev Plant Sci 33: 141–189. https://doi.org/10.1080/07352689.2014.870411
Jamroz E, Kocowicz A, Bekier J, et al. (2014) Properties of soil organic matter in Podzols under mountain dwarf pine (Pinus mugo Turra.) and Norway spruce (Picea abies (L.) Karst.) in various stages of dieback in the East Sudety Mountains, Poland. Forest Ecol Manag 330: 261–270 https://doi.org/10.1016/j.foreco.2014.07.020
Javid AD, Sundarapandian S (2015) Altitudinal variation of soil organic carbon stocks in temperate forests of Kashmir Himalayas, India. Environ Monit Assess 187: 11. https://doi.org/10.1007/s10661-014-4204-9
Khan MN, Mobin M, Abbas ZK, et al. (2016) Impact of varying elevations on growth and activities of antioxidant enzymes of some medicinal plants of Saudi Arabia. Acta Ecologica Sinica 36: 141–148. https://doi.org/10.1016/j.chnaes.2015.12.009
Kim HW, Kim JB, Cho SM, et al. (2012) Anthocyanin changes in the Korean purple-fleshed sweet potato, Shinzami, as affected by steaming and baking. Food Chem 130: 966–972. https://doi.org/10.1016/j.foodchem.2011.08.031
Kitajima K, Fox AM, Sato T, et al. (2006) Cultivar selection prior to introduction may increase invasiveness: evidence from Ardisia crenata. Biol. Invasions 8: 1471–1482. https://doi.org/10.1007/s10530-005-5839-9
Klára K, Pavel V, Urban M, et al. (2018) Plant abiotic stress proteomics: The major factors determining alterations in cellular proteome. Front Plant Sci 9: 122. https://doi.org/10.3389/fpls.2018.00122
Li H (2000) Theory and Techniques of Plant Physiology and Biochemistry experiments. Higher Education Press. pp 119–261. (In Chinese).
Liu F, Wang X, Chi Q, et al. (2021) Spatial variations in soil organic carbon, nitrogen, phosphorus contents and controlling factors across the “Three Rivers” regions of southwest China. Sci Total Environ 794: 148975. https://doi.org/10.1016/J.SCITOTENV.2021.148795
McCallum JA, Walker JRL (1990) Phenolic biosynthesis during grain development in wheat: changes in phenylalanine Ammonia-lyase activity and soluble phenolic content. J Cereal Sci 11: 35–49. https://doi.org/10.1016/S0733-5210(09)80179-3
McKinley DC, Rice CW, Blair JM (2008) Conversion of grassland to coniferous woodland has limited effects on soil nitrogen cycle processes. Soil Biol Biochem 40: 2627–2633. https://doi.org/10.1016/j.soilbio.2008.07.005
Moghimian N, Hosseini SM, Kooch Y, et al. (2017) Impacts of changes in land use/cover on soil microbial and enzyme activities. Catena 157: 407–414. https://doi.org/10.1016/j.catena.2017.06.003
Njeru CM, Ekesi S, Mohamed SA, et al. (2017) Assessing stock and thresholds detection of soil organic carbon and nitrogen along an altitude gradient in an east Africa mountain ecosystem. Geoderma Reg 10: 29–38. https://doi.org/10.1016/j.geodrs.2017.04.002
Nottingham AT, Turner BL, Whitaker J, et al. (2015) Soil microbial nutrient constraints along a tropical forest elevation gradient: a belowground test of a biogeochemical paradigm. Biogeosciences 12: 6071–6083. https://doi.org/10.5194/bg-12-6071-2015
Parras-Alcántara L, Lozano-García B, Galán-Espejo A (2015) Soil organic carbon along an altitudinal gradient in the Despeñaperros Natural Park, southern Spain. Solid Earth 6: 125–134. https://doi.org/10.5194/se-6-125-2015
Pavel MAA, A.Mukul S, Uddin MB, et al. (2016) Effects of stand characteristics on tree species richness in and around a conservation area of northeast Bangladesh. J Mt Sci 13: 1085–1095. https://doi.org/10.1007/s11676-018-0786-3
Pluess AR, Frei E, Kettle CJ, et al. (2011) Plant growth and fitness of Scabiosa columbaria under climate warming conditions. Plant Ecol Divers 4: 379–389. https://doi.org/10.1080/17550874.2011.618848
Purahong W, Durka W, Fischer M, et al. (2016) Tree species, tree genotypes and tree genotypic diversity levels affect microbe-mediated soil ecosystem functions in a subtropical forest. Sci Rep-UK 6: 36672. https://doi.org/10.1038/srep36672
Rahman IU, Afzal A, Iqbal Z, et al. (2019) Response of plant physiological attributes to altitudinal gradient: plant adaptation to temperature variation in the Himalayan region. Sci Total Environ 706: 135714. https://doi.org/10.1016/j.scitotenv.2019.135714
Rajsnerová P, Klem K, Holub P, et al. (2015) Morphological, biochemical and physiological traits of upper and lower canopy leaves of European beech tend to converge with increasing altitude. Tree physiol 35: 47–60. https://doi.org/10.1093/treephys/tpu104
Rathore N, Thakur D, Chawla A (2018) Seasonal variations coupled with elevation gradient drives significant changes in eco-physiological and biogeochemical traits of a high altitude evergreen broadleaf shrub, Rhododendron anthopogon. Plant Physiol Bioch 132: 708–719 https://doi.org/10.1016/j.plaphy.2018.08.009
Ren CJ, Kang D, Wu JP, et al. (2016) Temporal variation in soil enzyme activities after afforestation in the Loess Plateau, China. Geoderma 282: 103–111. https://doi.org/10.1016/j.geoderma.2016.07.018
Ren J, Dai W, Yang C, et al. (2018) Physiological regulation of poplar species to experimental warming differs between species with contrasting elevation ranges. New Forest 49: 329–340. https://doi.org/10.1007/s11056-017-9622-4
Ruelland E, Vaultier M-N, Zachowski A, et al. (2009) Chapter 2 Cold Signalling and Cold Acclimation in Plants. Adv Bot Res 49: 35–150. https://doi.org/10.1016/S0065-2296(08)00602-2
Santiago JHd, Lucas-Borja ME, Wic-Baena C, et al. (2016) Effects of thinning and induced drought on microbiological soil properties and plant species diversity at dry and semiarid locations. Land Degrad Dev 27: 1151–1162. https://doi.org/10.1002/ldr.2361
Shi Z, Haworth M, Feng Q, et al. (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: 115. https://doi.org/10.1093/aobpla/plv115
Tan Q, Wang G (2016) Decoupling of nutrient element cycles in soil and plants across an altitude gradient. Sci rep 6: 34875. https://doi.org/10.1038/srep34875
Terfa MT, Roro AG, Olsen JE, et al. (2014) Effects of UV radiation on growth and postharvest characteristics of three pot rose cultivars grown at different altitudes. Sci Hortic-Amsterdam 178: 184–191. https://doi.org/10.1016/j.scienta.2014.08.021
Tsozué D, Nghonda JP, Tematio P, et al. (2019) Changes in soil properties and soil organic carbon stocks along an elevation gradient at Mount Bambouto, Central Africa. Catena 175: 251–262. https://doi.org/10.1016/j.catena.2018.12.028
Wang B, Xue S, Liu GB, et al. (2012) Changes in soil nutrient and enzyme activities under different vegetations in the Loess Plateau area, Northwest China. Catena 92: 186–195. https://doi.org/10.1016/j.catena.2011.12.004
Wang L, Zhang G, Zhu P, et al. (2022) Soil C, N and P contents and their stoichiometry as affected by typical plant communities on steep gully slopes of the Loess Plateau, China. Catena 208. https://doi.org/10.1016/J.CATENA.2021.105740
Wellburn A, Lichtenthaler H (1984) Formulae and program to determine total carotenoids and chlorophylls A and B of leaf extracts in different solvents. Adv Photosynth Res 9–12. https://doi.org/10.1007/978-94-017-6368-4_3
Xiao L, Li P, Shi P, et al. (2019) Soil nutrient stoichiometries and enzymatic activities along an elevational gradient in the dry-hot valley region of southwestern China. Arch Agron Soil Sci 65: 322–333. https://doi.org/10.1080/03650340.2018.1502882
Xu H, Qu Q, Lu B, et al. (2020) Response of soil specific enzyme activity to vegetation restoration in the Loess hilly region of China. Catena 191: 104564. https://doi.org/10.1016/j.catena.2020.104564
Yang S, Zhao W, Pereira P (2020) Determinations of environmental factors on interactive soil properties across different land-use types on the Loess Plateau, China. Sci Total Environ 738: 140270. https://doi.org/10.1016/j.scitotenv.2020.140270
Yang Y, Zhang L, Li H, et al. (2018) Soil physicochemical properties and vegetation structure along an elevation gradient and implications for the response of alpine plant development to climate change on the northern slopes of the Qilian Mountains. J Mt Sci 15: 1006–1019. https://doi.org/10.1007/s11629-017-4637-z
Zhang S, Chen D, Sun D, et al. (2012) Impacts of altitude and position on the rates of soil nitrogen mineralization and nitrification in alpine meadows on the eastern Qinghai-Tibetan Plateau, China. Biol Fert Soils 48: 393–400. https://doi.org/10.1007/s00374-011-0634-5
Zhang X, Feng Q, Cao J, et al. (2022) Response of leaf stoichiometry of Potentilla anserina to elevation in China’s Qilian Mountains. Front Plant Sci. https://doi.org/10.3389/FPLS.2022.941357
Zhou J, Wu Y, Bing H, et al. (2016) Variations in soil phosphorus biogeochemistry across six vegetation types along an altitudinal gradient in SW China. Catena 142: 102–111. https://doi.org/10.1016/j.catena.2016.03.004
Zhu P, Yang L (2014) Ambient UV-B radiation inhibits the growth and physiology of Brassica napus L. on the Qinghai-Tibetan plateau. Field Crop Res 171: 79–85. https://doi.org/10.1016/j.fcr.2014.11.006
Zinn YL, Andrade AB, Araujo MA, et al. (2018) Soil organic carbon retention more affected by altitude than texture in a forested mountain range in Brazil. Soil Res 56: 284. https://doi.org/10.1071/SR17205
Acknowledgments
The research supported by the Doctoral Research Fund Project of Southwest Forestry University (CN) (Grant No. 111806). We thank three anonymous reviewers for their helpful comments on improving our manuscript and editorial office of JMS for providing handing. Acknowledge Dr. Fiona Barnett, who proofread our paper.
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Ai, Xm., Li, Y., Xie, H. et al. Adaptive mechanisms of Ardisia crenata var. bicolor along an elevational gradient on Gaoligong Mountain, Southwest China. J. Mt. Sci. 20, 765–778 (2023). https://doi.org/10.1007/s11629-022-7369-7
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DOI: https://doi.org/10.1007/s11629-022-7369-7