Abstract
Karst ecosystems are formed by dissolution of soluble rocks, usually with conspicuous landscape features, such as sharp peaks, steep slopes and deep valleys. The plants in karst regions develop special adaptability. Here, we reviewed the research progresses on plant adaptability in karst regions, including drought, high temperature and light, high-calcium stresses responses and the strategies of water utilization for plants, soil nutrients impact, human interference and geographical traits on karst plants. Drought, high temperature and light change their physiological and morphological structures to adapt to karst environments. High-calcium and soil nutrients can transfer surplus nutrients to special parts of plants to avoid damage of high nutrient concentration. Therefore, karst plants can make better use of limited water. Human interference also affects geographical distribution of karst plants and their growing environment. All of these aspects may be analyzed to provide guidance and suggestions for related research on plant adaptability mechanisms.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abreu ME, Munné-Bosch S (2008) Salicylic acid may be involved in the regulation of drought-induced leaf senescence in perennials: a case study in field-grown Salvia officinalis L. plants. Environ Exp Bot 64:105–112. https://doi.org/10.1016/j.envexpbot.2007.12.016
Adams WW III, Demmig-Adams B, Logan BA, Barker DH, Osmond CB (1999) Rapid changes in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines, Stephania japonica and Smilax australis, growing in the understorey of an open Eucalyptus forest. Plant Cell Environ 22:125–136
Bai K, Lv S, Ning S, Zeng D, Guo Y, Wang B (2019) Leaf nutrient concentrations associated with phylogeny, leaf habit and soil chemistry in tropical karst seasonal rainforest tree species. Plant Soil 434:305–326. https://doi.org/10.1007/s11104-018-3858-4
Baker NR (1996) Photoinhibition of photosynthesis. In: Jennings RC, Zucchelli G, Ghetti F, Colombetti G (eds) Light as energy source and information carrier in plant physiology. Plenum Press, New York, pp 89–96. https://doi.org/10.1007/978-1-4613-0409-8_7
Barbeta A, Mejía-Chang M, Ogaya R, Voltas J, Dawson T, Peñuelas J (2015) The combined effects of a long-term experimental drought and an extreme drought on the use of plant-water sources in a Mediterranean forest. Global Change Biol 21:1213–1225. https://doi.org/10.1111/gcb.12785
BatisticO KJ (2012) Analysis of calcium signaling pathways in plants. Biochim Biophys Acta 1820:1283–1293. https://doi.org/10.1016/j.bbagen.2011.10.012
Bátori Z, Vojtkó A, Maák I, Lőrinczi G, Farkas T, Kántor N, Tanács E, Kiss P, Juhász O, Módra G, Tölgyesi C, Erdős L, Aguilon D, Keppel G (2019) Karst dolines provide diverse microhabitats for different functional groups in multiple phyla. Sci Rep. https://doi.org/10.1038/s41598-019-43603-x
Berteotti S, Ballottari M, Bassi R (2016) Increased biomass productivity in green algae by tuning non-photochemical quenching. Sci Rep 6:21339. https://doi.org/10.1038/s41598-019-48482-w
Borer CH, Hamby MN, Hutchinson LH (2012) Plant tolerance of a high calcium environment via foliar partitioning and sequestration. J Arid Environ 85:128–131. https://doi.org/10.1016/j.jaridenv.2012.06.004
Bothwel J, Ng C (2005) The evolution of Ca2+ signalling in photosynthetic eukaryotes. New Phytol 166:21–38. https://doi.org/10.1111/j.1469-8137.2004.01312.x
Burstrom HG (1968) Calcium and plant growth. Biol Rev 43:287–316. https://doi.org/10.1111/j.1469-185X.1968.tb00962.x
Carafoli E, Santella L, Branca D, Brini M (2001) Generation, control, and processing of cellular calcium signals. Crit Rev Biochem Mol Biol 36:107–260. https://doi.org/10.1080/20014091074183
Carriere SD, Martin-StPau NK, Cakpo CB, Patris N, Gillon M, Chalikakis K, Doussan C, Olioso A, Babic M, Jouineau A, Simioni G, Davi H (2020) The role of deep vadose zone water in tree transpiration during drought periods in karst settings—insights from isotopic tracing and leaf water potential. Sci Total Environ 699:134332. https://doi.org/10.1016/j.scitotenv.2019.134332
Chen CS, Xie ZX, Liu XJ (2009) Dynamic transformation of the substances of osmotic adjustment in winter wheat under iso-osmotic salt and drought stresses. Bull Bot Res 17:777–780
Chen YJ, Cao KF, Schnitzer SA, Fan ZX, Zhang JL, Bongers F (2015) Water-use advantage for lianas over trees in tropical seasonal forests. New Phytol 205:128–136. https://doi.org/10.1111/nph.13036
Chen T, Peng L, Liu SQ, Wang Q (2017) Land cover change in different altitudes of Guizhou–Guangxi karst mountain area, China: patterns and drivers. J Mt Sci 14:1873–1888. https://doi.org/10.1007/s11629-016-4202-1
Chen J, Yu J, Bai X, Zeng WJ (2020) Fragility of karst ecosystem and environment: long-term evidence from lake sediments. Agric Ecosyst Environ 294:7. https://doi.org/10.1016/j.agee.2020.106862
Cheng XF, Li SY, Hu H, Wu TG (2011) Leaf traits of orchids in relation to life form in Karst area of southwestern China. Plant Divers Resour 33:595–604. https://doi.org/10.3724/sp.j.1143.2011.11067
Chi Y, Xiong K, Zhang Z (2016) Research on photosynthetic interannual dynamics of gramineous forage in the karst rocky desertification regions of south China. Oxid Commun 39:2476–2496
Crous K, O’Sullivan O, Zaragoza-Castells J, Bloomfield K, Negrini A, Meir P, Turnbull M, Griffin K, Atkin O (2017) Nitrogen and phosphorus availabilities interact to modulate leaf trait scaling relationships across six plant functional types in a controlled-environment study. New Phytol 215:992–1008. https://doi.org/10.1111/nph.14591
Cui BS, Zhai HJ, Dong SK, Chen B, Liu SL (2009) Multivariate analysis of the effects of edaphic and topographical factors on plant distribution in the Yilong Lake Basin of Yun-Gui Plateau, China. Can J Plant Sci 89:209–219. https://doi.org/10.4141/CJPS08013
Cui Q, Wu H, Shen S, Xu Y, Ye G (2015) Chinese karst geology and measures to prevent geohazards during shield tunnelling in karst region with caves. Nat Hazards 77:129–152. https://doi.org/10.1007/s11069-014-1585-6
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679. https://doi.org/10.1146/annurev-arplant-042809-112122
Dang C, Li Z, Chen M, Gao T, Huang H, Liu J, Tao J (2018) Physiological and biochemical characteristics of epilithic moss Homomallium simlaense (Mitt.) Broth. Mitt under high temperature and drought stress. J Plant Sci 36:393–401. https://doi.org/10.11913/psj.2095-0837.2018.30393
Davies E (2004) New functions for electrical signals in plants. New Phytol 161:607–612
Dayod M, Tyerman SD, Leigh RA, Gilliham M (2010) Calcium storage in plants and the implications for calcium biofortification. Protoplasma 247:215–231. https://doi.org/10.1007/s00709-010-0182-0
Deng Y, Jiang ZC, Cao JH, Li Q, Lan FN (2004) Characteristics comparison of the leaf anatomy of Cyclobalanopsis glauca and its adaption to the environment of typical karst peak cluster areas in Nongla. Guihaia 24:317–322 (in Chinese)
Derks AK, Bruce D (2018) Rapid regulation of excitation energy in two pennate diatoms from contrasting light climates. Photosynth Res 138:149–165. https://doi.org/10.1007/s11120-018-0558-0
Evaristo J, McDonnell J (2017) Prevalence and magnitude of groundwater use by vegetation: a global stable isotope meta-analysis. Sci Rep 7:44110. https://doi.org/10.1038/srep44110
Fan Z, Bräuning A, Thomas A, Li J, Cao K (2011) Spatial and temporal temperature trends on the Yunnan Plateau (southwest China) during 1961–2004. Int J Climatol 31:2078–2090. https://doi.org/10.1002/joc.2214
Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166. https://doi.org/10.1199/tab.0166
Fu P, Liu W, Fan Z, Cao K (2016) Is fog an important water source for woody plants in an Asian tropical karst forest during the dry season? Ecohydrology 9:964–972. https://doi.org/10.1002/eco.1694
Fu PL, Zhu SD, Zhang JL, Finnegan PM, Jiang YJ, Lin H, Fan ZX, Cao KF (2019) The contrasting leaf functional traits between a karst forest and a nearby non-karst forest in south-west China. Funct Plant Biol 46:907–915. https://doi.org/10.1071/FP19103
Fujii H, Zhu J (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385. https://doi.org/10.1073/pnas.0903144106
Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19:485–494. https://doi.org/10.1105/tpc.106.048538
Furuichi T, Kawano T, Tatsumi H, Sokabe M (2007) Roles of ion channels in environmental responses of plants. In: Martinac B (ed) Sensing with ion channels. Springer series in biophysics. Springer, Heidelberg, pp 47–67
Geekiyanage N, Goodale U, Cao K, Kitajima K (2019) Plant ecology of tropical and subtropical karst ecosystems. Biotropica 51:626–640. https://doi.org/10.1111/btp.12696
Goss R, Lepetit B (2014) Biodiversity of NPQ. J Plant Physiol 172:13–32. https://doi.org/10.1016/j.jplph.2014.03.004
Grams TEE, Lautner S, Felle HH, Matyssek R, Fromm J (2009) Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf. Plant Cell Environ 32:319–326. https://doi.org/10.1111/j.1365-3040.2008.01922.x
Grieco M, Roustan V, DermendjievG RS, Jain A, Leonardelli M, Neumann K, Berger V, Engelmeier D, Bachmann G et al (2020) Adjustment of photosynthetic activity to drought andfluctuating light in wheat. Plant Cell Environ 43:1484–1500. https://doi.org/10.1111/pce.13756
GuoYY YuHY, Yang MM, Kong DS, Zhang YJ (2018) Effect of drought stress on lipid peroxidation, osmotic adjustment and antioxidant enzyme activity of leaves and roots of Lycium ruthenicum murr. seedling. Russ J Plant Physiol 65:244–250. https://doi.org/10.1134/S1021443718020127
Gutiérrez F, Parise M, De Waele J, Jourde H (2014) A review on natural and human-induced geohazards and impacts in karst. Earth Sci Rev 138:61–88. https://doi.org/10.1016/j.earscirev.2014.08.002
Hao Z, Kuang Y, Kang M (2015) Untangling the influence of phylogeny, soil and climate on leaf element concentrations in a biodiversity hotspot. Funct Ecol 29:165–176. https://doi.org/10.1111/1365-2435.12344
Hepler P (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142. https://doi.org/10.1105/tpc.105.032508
Hetherington AM, Brownlee C (2004) The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55:401–427. https://doi.org/10.1146/annurev.arplant.55.031903.141624
Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052. https://doi.org/10.1111/j.1365-313X.2010.04124.x
Hlaváčková V, Krchňák P, Nauš J, Novák O, Špundová M, Strnad M (2006) Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta 225:235–244. https://doi.org/10.1007/s00425-006-0325-x
Hlavinka J, Nozkova-Hlavackova V, Flokova K, Novak O, Naus J (2012) Jasmonic acid accumulation and systemic photosynthetic and electrical changes in locally burned wild type tomato, ABA-deficient sitiens mutants and sitiens pre-treated by ABA. Plant Physiol Biochem 54:89–96. https://doi.org/10.1016/j.plaphy.2012.02.014
Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43:8281–8289
Hong-Bo S, Li-Ye C, Ming-An S (2008) Calcium as a versatile plant signal transducer under soil water stress. BioEssays 30:634–641. https://doi.org/10.1002/bies.20770
Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684. https://doi.org/10.1146/annurev.arplant.47.1.655
Hu H, Xiong L (2014) Genetic engineering and breeding of drought-resistant crops. Annu Rev Plant Biol 65:715–741. https://doi.org/10.1146/annurev-arplant-050213-040000
Illan JG, Gutierrez D, Wilson RJ (2010) Fine-scale determinants of butterfly species richness and composition in a mountain region. J Biogeogr 37:1706–1720. https://doi.org/10.1111/j.1365-2699.2010.02314.x
Irving HR, Gehring CA, Parish RW (1992) Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc Natl Acad Sci USA 89:1790–1794. https://doi.org/10.1073/pnas.89.5.1790
Jarrett HW, Brown CJ, Black CC, Cormier MJ (1982) Evidence that calmodulin is in the chloroplast of peas and serves a regulatory role in photosynthesis. J Biol Chem 257:13795–13804
Ji F, Li N, Deng X (2009) Calcium contents and high calcium adaptation of plants in karst area of China. Chin J Plant Ecol 33:926–935. https://doi.org/10.3773/j.issn.1005-264x.2009.05.012
Jiang Z, Lian Y, Qin X (2014) Rocky desertification in Southwest China: impacts, causes, and restoration. Earth Sci Rev 132:1–12. https://doi.org/10.1016/j.earscirev.2014.01.005
Jiang Y, Bai K, Guo Y, Wang B, Li D, Li X, Liu Z (2016) Floral traits of woody plants and their habitat differentiations in a northern tropical karst forest. Biodivers Sci 24:148–156
Jin W, Long Y, Fu C, Zhang L, Xiang J, Wang B, Li M (2018) Ca2+ imaging and gene expression profiling of Lonicera Confusa in response to calcium-rich environment. Sci Rep 8:10. https://doi.org/10.1038/s41598-018-25611-5
Jones W, White W (2019) Karst. In: White WB, Culver DC, Pipan T (eds) Encyclopedia of caves, 3rd edn. Academic Press, pp 609–618. https://doi.org/10.1016/B978-0-12-814124-3.00072-8
Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357. https://doi.org/10.1105/tpc.010362
Kang J, Hwang J, Lee M, Kim Y, Assmann SM, Martinoia E et al (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci USA 107:2355–2360. https://doi.org/10.1073/pnas.0909222107
Karapetyan NV (2007) Non-photochemical quenching of fluorescence in cyanobacteria. Biochemistry 72:1127–1135. https://doi.org/10.1134/S0006297907100100
Khajuria M, Rahulbc VP, Vyas D (2020) Photochemical efficiency is negatively correlated with the Δ9-tetrahydrocannabinol content in Cannabis sativa L. Plant Physiol Biochem 151:589–600. https://doi.org/10.1016/j.plaphy.2020.04.003
Kikuyama M, Tazawa M (1983) Transient increase of intracellular Ca2+ during excitation on tonoplast-free Chara cells. Protoplasma 117:62–67
Kim JB, Kang JY, Kim SY (2004) Over-expression of a transcription factor regulating ABA-responsive gene expres-sion confers multiple stress tolerance. Plant Biotechnol J 2:459–466. https://doi.org/10.1111/j.1467-7652.2004.00090.x
Kim T, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591. https://doi.org/10.1146/annurev-arplant-042809-112226
Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D et al (2008) Ascorbate peroxidase1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203. https://doi.org/10.1074/jbc.M806337200
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349. https://doi.org/10.1146/annurev.pp.42.060191.001525
Kudoyarova GR, Dodd IC, Veselov DS, Rothwell SA, Veselov YS (2015) Common and specific responses to availability of mineral nutrients and water. J Exp Bot 66:2133–2144. https://doi.org/10.1093/jxb/erv017
Kulik A, Wawer I, Krzywińska E, Bucholc M, Dobrowolska G (2011) SnRK2 protein kinases—key regulators of plant response to abiotic stresses. OMICS 15:859–872. https://doi.org/10.1089/omi.2011.0091
Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A et al (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci USA 107:2361–2366. https://doi.org/10.1073/pnas.0912516107
Legrand H (1973) Hydrological and ecological problems of karst regions. Science 179:859–864. https://doi.org/10.1126/science.179.4076.859
Leng G, Hall J (2019) Crop yield sensitivity of global major agricultural countries to droughts and the projected changes in the future. Sci Total Environ 654:811–821. https://doi.org/10.1016/j.scitotenv.2018.10.434
Leuschner C, Moser G, Bertsch C, Röderstein M, Hertel D (2007) Large altitudinal increase in tree root/shoot ratio in tropical mountain forests of Ecuador. Basic Appl Ecol 8:219–230
Levin G, Kulikovsky S, Liveanu V, Eichenbaum B, Meir A, Isaacson T, Tadmor Y, Adir N, Schuster G (2021) The desert green algae Chlorella ohadii thrives at excessively high light intensities by exceptionally enhancing the mechanisms that protect photosynthesis from photoinhibition. Plant J. https://doi.org/10.1111/tpj.15232
Li EX, Jiang ZC, Cao JH, Jiang GH, Deng Y (2004) The comparison of properties of Karst soil and Karst erosion ratio under different successional stages of Karst vegetation in Nongla, Guangxi. Acta Ecol Sinica 24:1131–1139 (in Chinese with English abstract)
Li Q, Yu LJ, Deng Y, Li W, Li M, Cao J (2007) Leaf epidermal characters of Lonicera japonica and Lonicera confusa and their ecology adaptation. J for Res 18:103–108. https://doi.org/10.1007/s11676-007-0020-1
Li X, Liu C, Harue M, Li S, Liu X (2010) The use of environmental isotopic (C, Sr, S) and hydrochemical tracers to characterize anthropogenic effects on karst groundwater quality: a case study of the Shuicheng Basin, SW China. Appl Geochem 25:1924–1936. https://doi.org/10.1016/j.apgeochem.2010.10.008
Li HY, Luo HJ, Li DY, Hu T, Fu JM (2012) Antioxidant enzyme activity and gene expression in response to lead stress in Perennial Ryegrass. J Am Soc Hort Sci 137:80–85. https://doi.org/10.21273/JASHS.137.2.80
Li W, Xu F, Chen S, Zhang Z, Zhao Y, Jin Y, Li M, Zhu Y, Liu Y, Yang Y, Deng X (2014) A comparative study on Ca content and distribution in two Gesneriaceae species reveals distinctive mechanisms to cope with high rhizospheric soluble calcium. Front Plant Sci 5:647. https://doi.org/10.3389/fpls.2014.00647
Li Z, Xu X, Yu B, Xu C, Liu M, Wang K (2016) Quantifying the impacts of climate and human activities on water and sediment discharge in a karst region of southwest China. J Hydrol 542:836–849. https://doi.org/10.1016/j.jhydrol.2016.09.049
Li D, Wen L, Yang L, Luo P, Xiao K, Chen H, Zhang W, He X, Chen H, Wang K (2017a) Dynamics of soil organic carbon and nitrogen following agricultural abandonment in a karst region. J Geophys Res Biogeosci 122(1):230–242. https://doi.org/10.1002/2016jg003683
Li J, Li Z, Liu Q, Wang P, Hu S (2017b) Nutrient absorption, accumulation, and distribution characteristics of three excellent native tree species plantations in karst area of western Hunan. Shengtaixue Zazhi 36:902–909. https://doi.org/10.13292/j.1000-4890.201704.019
Li F, He X, Sun Y, Zhang X, Tang X, Li Y, Yi Y (2019a) Distinct endophytes are used by diverse plants for adaptation to karst regions. Sci Rep 9:5246. https://doi.org/10.1038/s41598-019-41802-0
Li R, Wu Q, Zhang J, Wen Y, Li (2019b) Effects of land use change of sloping farmland on characteristic of soil erosion resistance in typical karst mountainous areas of southwestern China. Pol J Environ Study 28:2707–2716. https://doi.org/10.15244/pjoes/94288
Liang KM, Lin ZF, Liu N, Zhang QM, Wang J, Wang ZF, Guan LL (2010) Characteristics of sun- and shade-adapted populations of an endangered plant Primulina tabacum Hance. Photosynthetica 48:494–506. https://doi.org/10.1007/s11099-010-0066-8
Lieberman D, Lieberman M, Peralta R, Hartshorn GS (1996) Tropical forest structure and composition on a large-scale altitudinal gradient in Costa Rica. J Ecol 84:137–152
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136. https://doi.org/10.1146/annurev.arplant.57.032905.105316
Liu CC, Liu YG, Guo K, Zheng YR, Li GQ, Yu LF et al (2010) Influence of drought intensity on the response of six woody karst species subjected to successive cycles of drought and rewatering. Physiol Plant 139:39–54. https://doi.org/10.1111/j.1399-3054.2009.01341.x
Liu C, Liu Y, Guo K, Fan D, Li G, Zheng Y, Yu L, Yang R (2011) Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environ Exp Bot 71:174–183. https://doi.org/10.1016/j.envexpbot.2010.11.012
Liu JY, Fu PL, Wang YJ, Cao KF (2012) Different drought-adaptation strategies as characterized by hydraulic and water-relations traits of evergreen and deciduous figs in a tropical karst forest. Plant Sci J 30:484–493. https://doi.org/10.3724/sp.j.1142.2012.50484
Liu B, Chen C, Lian Y, Chen J, Chen X (2015) Long-term change of wet and dry climatic conditions in the southwest karst area of China. Glob Planet Change 127:1–11. https://doi.org/10.1016/j.gloplacha.2015.01.009
Liu M, Xu X, Wang D, Sun A, Wang K (2016) Karst catchments exhibited higher degradation stress from climate change than the non-karst catchments in southwest China: an ecohydrological perspective. J Hydrol 535:173–180. https://doi.org/10.1016/j.jhydrol.2016.01.033
Liu Q, Deng D, Yao B et al (2020a) Analysis of the karst springs’ supply sources in rocky desertification area of Guanling–Huajiang, Guizhou China. Carbonates Evaporites 35:9. https://doi.org/10.1007/s13146-020-00623-3
Liu Y, Wei X, Zhou Z, Shao C, Su S (2020b) Influence of heterogeneous karst microhabitats on the root foraging ability of Chinese Windmill Palm (Trachycarpus fortunei) seedlings. Int J Environ Res Public Health 17:15. https://doi.org/10.3390/ijerph17020434
Lu YR (2012) Karst in China: a world of improbable peaks and wonderful caves. Higher Educ Press
Lusk CH, Reich PB, Montgomery RA, Ackerly DD, Cavender-Bares J (2008) Why are evergreen leaves so contrary about shade? Trends Ecol Evol 23:299–303. https://doi.org/10.1016/j.tree.2008.02.006
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068. https://doi.org/10.1126/science.1172408
Malliarakis D, Tsiavos T, Ioannidis NE, Kotzabasis K (2015) Spermine and lutein quench chlorophyll fluorescence in isolated PSII antenna complexes. J Plant Physiol 183:108–113. https://doi.org/10.1016/j.jplph.2015.06.006
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
Meng H, Zhang W, Zhang G, Wang J, Meng Z, Long G, Yang S (2018) Unigene-based RNA-seq provides insights on drought stress responses in Marsdenia tenacissima. PLoS ONE 13:e0202848. https://doi.org/10.1371/journal.pone.0202848
Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566. https://doi.org/10.1104/pp.125.4.1558
Müller MN, Barcelos e Ramos J, Schulz KG, Riebesell U, Kaźmierczak J, Gallo F, Mackinder L, Li Y, Nesterenko PN, Trull TW et al (2015) Phytoplankton calcification as an effective mechanism to alleviate cellular calcium poisoning. Biogeosciences 12:6493–6501. https://doi.org/10.5194/bg-12-6493-2015
Munné-Bosch S, Peñuelas J (2003) Photo- and antioxidative protection during summer leaf senescence in Pistacia lentiscus L. grown under Mediterranean field conditions. Ann Bot 92:385–391
Munné-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31:203–216. https://doi.org/10.1071/FP03236
Murata N, Takahashi S, Nishiyama S, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421. https://doi.org/10.1016/j.bbabio.2006.11.019
Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92
Murchie EH, Ruban AV (2019) Dynamic non-photochemical quenching in plants: From molecular mechanism to productivity. Plant J 101:885–896. https://doi.org/10.1111/tpj.14601
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185. https://doi.org/10.1146/annurev.arplant.56.032604.144046
Nardini A, Casolo V, Dal Borgo A, Savi T, Stenni B, Bertoncin P, Zini L, McDowell N (2016) Rooting depth, water relations and non-structural carbohydrate dynamics in three woody angiosperms differentially affected by an extreme summer drought. Plant Cell Environ 39:618–627. https://doi.org/10.1111/pce.12646
Ni LK, Gu DX, He W, Huang YQ, Chen ZY (2019) Research advances in plant ecological adaptability in karst area. Shengtaixue Zazhi 38:2210–2217. https://doi.org/10.13292/j.1000-4890.201907.033
Nishimura N, Sarkeshik A, Nito K, Park S, Wang A, Carvalho PC et al (2010) PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61:290–299. https://doi.org/10.1111/j.1365-313X.2009.04054.x
Noctor G, Ruban AV, Horton P (1993) Modulation of ΔpH-dependent nonphotochemical quenching of chlorophyll fluorescence in spinach chloroplasts. Biochim Biophys Acta 1183:339–344. https://doi.org/10.1016/0005-2728(93)90237-A
Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071. https://doi.org/10.1126/science.1173041
Pearcy RW (1977) Acclimation of photosynthetic and respiratory carbon dioxide exchange to growth temperature in Atriplex lentiformis (Torr) Wats. Plant Physiol 59:795–799. https://doi.org/10.1104/pp.59.5.795
Peng X, Dai Q, Ding G, Li C (2019) Role of underground leakage in soil, water and nutrient loss from a rock-mantled slope in the karst rocky desertification area. J Hydrol 578:124086. https://doi.org/10.1016/j.jhydrol.2019.124086
Powles S (1984) Photoinhibition of photosynthesis induced by visible light. Ann Rev Plant Physiol 35:15–44. https://doi.org/10.1146/annurev.pp.35.060184.000311
Ranjev R, Thuleaua P, Schroederb JI (1993) Signal transduction and calcium channels in higher plants. Curr Opin Biotechnol 4:172–176. https://doi.org/10.1093/jxb/eri302
Reddy VS, Reddy AS (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65:1745–1776. https://doi.org/10.1016/j.phytochem.2004.04.033
Rivas-Ubach A, Gargallo-Garriga A, Sardans J, Oravec M, Mateu-Castell L, Perez-Trujillo M, Parella T, Ogaya R, Urban O, Penuelas J (2014) Drought enhances folivory by shifting foliar metabolomes in Quercus ilex trees. New Phytol 202:874–885. https://doi.org/10.1111/nph.12687
Rong L, Wang SJ, Liu N, Yang L (2005) Leaf anatomical characters and its ecological adaptation of the pioneer species in the karst mountain area-with a special reference to the Huajiang Canyon of Guizhou. J Mount Sci 23:35–42 (in Chinese)
Ruban AV, Johnson MP (2009) Dynamics of higher plant photosystem cross-section associated with state transitions. Photosynth Res 99:173–183
Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta Bioenerg 1817:167–181. https://doi.org/10.1016/j.bbabio.2011.04.007
Sauro U (2012) Closed depressions in karst areas. In: White WB, Culver DC (eds) Encyclopedia of caves, 2nd edn. Academic Press, Amsterdam, pp 140–155. https://doi.org/10.1016/B978-0-12-383832-2.00133-X
Savi T, Petruzzellis F, Moretti E, Stenni B, Zini L, Martellos S, Lisjak K, Nardini A (2019) Grapevine water relations and rooting depth in karstic soils. Sci Total Environ 692:669–675. https://doi.org/10.1016/j.scitotenv.2019.07.096
Schaller J, Paschold PJ (2009) Stomata-characteristics and responses to soil drought indicating a cultivar specific drought stress susceptibility in asparagus. Eur J Hortic Sci 74:145–151
Seki M, Taishi U, Kaoru U, Kazuo S (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302. https://doi.org/10.1016/j.pbi.2007.04.014
Selman M, Greenhalgh S, Diaz R, Sugg Z (2008) Eutrophication and hypoxia in coastal areas: a global assessment of the state of knowledge. World Resour Inst 284:1–6
Sluchanko NN, Slonimskiy YB, Shirshin EA, Moldenhauer M, Friedrich T, Maksimov EG (2018) OCP-FRP protein complex topologies suggest a mechanism for controlling high light tolerance in cyanobacteria. Nat Commun 9:3869
Sonani RR, Gardiner A, Rastogi RP, Cogdell R, Robert B, Madamwar D (2018) Site, trigger, quenching mechanism and recovery of non-photochemical quenching in cyanobacteria: recent updates. Photosynth Res 137:171–180. https://doi.org/10.1007/s11120-018-0498-8
Spalding EP, Harper JF (2011) The ins and outs of cellular Ca2+ transport. Curr Opin Plant Biol 14:715–720. https://doi.org/10.1016/j.pbi.2011.08.001
Sreenivasulu N, Harshavardhan VT, Govind G, Seiler C, Kohli A (2012) Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506:265–273. https://doi.org/10.1016/j.gene.2012.06.076
Sukhov V (2016) Electrical signals as mechanism of photosynthesis regulation in plants. Photosynth Res 130:373–387. https://doi.org/10.1007/s11120-016-0270-x
Sukhov V, Surova L, Sherstneva O, Vodeneev V (2014) Influence of variation potential on resistance of the photosynthetic machinery to heating in pea. Physiol Plant 152:773–783. https://doi.org/10.1111/ppl.12208
Sukhov V, Surova L, Sherstneva O, Bushueva A, Vodeneev V (2015) Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea. Funct Plant Biol 42:727–736. https://doi.org/10.1071/FP15052
Sukhov V, Gaspirovich V, Mysyagin S, Vodeneev V (2017) High-temperature tolerance of photosynthesis can be linked to local electrical responses in leaves of pea. Front Physiol 8:763. https://doi.org/10.3389/fphys.2017.00763
Sukhov V, Sukhova E, Gromova E, Surova L, Nerush V, Vodeneev V (2019) The electrical signal-induced systemic photosynthetic response is accompanied by changes in the photochemical reflectance index in pea. Funct Plant Biol 46:328–338. https://doi.org/10.1071/FP18224
Sukhova E, Akinchits E, Sukhov V (2017) Mathematical models of electrical activity in plants. J Membr Biol 250:407–423. https://doi.org/10.1007/s00232-017-9969-7
Sukhova E, Mudrilov M, Vodeneev V, Sukhov V (2018) Influence of the variation potential on photosynthetic flows of light energy and electrons in pea. Photosynth Res 136:215–228. https://doi.org/10.1007/s11120-017-0460-1
Surova L, Sherstneva O, Vodeneev V, Katicheva L, Semina M, Sukhov V (2016a) Variation potential-induced photosynthetic and respiratory changes increase ATP content in pea leaves. J Plant Physiol 202:57–64. https://doi.org/10.1016/j.jplph.2016.05.024
Surova L, Sherstneva O, Vodeneev V, Sukhov V (2016b) Variation potential propagation decreases heat-related damage of pea photosystem I by 2 different pathways. Plant Signal Behav 11:e1145334. https://doi.org/10.1080/15592324.2016.1145334
Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51. https://doi.org/10.1111/j.0031-9317.2005.00582.x
Swaffer B, Holland K, Doody T, Li C, Hutson J (2014) Water use strategies of two co-occurring tree species in a semi-arid karst environment. Hydrol Process 28:2003–2017. https://doi.org/10.1002/hyp.9739
Tang RJ, Luan S (2017) Regulation of calcium and magnesium homeostasis in plants: from transporter to signaling network. Curr Opin Plant Biol 39:97–105. https://doi.org/10.1016/j.pbi.2017.06.009
Tang C, Du H, Song T, Peng W, Zeng F, Yang G, Liang Z, Lu C (2013) Spatial heterogeneity of soil nitrogen and phosphorus under different land use patterns in depressions between karst hills. Chin J Ecol 32:1683–1689
Tang Q, Cheng X, Wei Y (2018) Study on species diversity of epiphyllous liverworts in karst region of Guangxi-Vietnam border. J Tropical Subtropical Bot 26:481–489. https://doi.org/10.11926/jtsb.3870
Tao J, Feng C, Ai B, Kang M (2016) Adaptive molecular evolution of the two-pore channel 1 gene TPC1 in the karst-adapted genus Primulina (Gesneriaceae). Ann Bot 118:1257–1268. https://doi.org/10.1093/aob/mcw168
Tian XJ (2007) Heat stress and plant thermotolerace. J Honghe Univ 5:7–9. https://doi.org/10.13963/j.cnki.hhuxb.2007.05.010
Toscano S, Farieri E, Ferrante A, Romano D (2016) Physiological and biochemical responses in two ornamental shrubs to drought stress. Front Plant Sci 7:645. https://doi.org/10.3389/fpls.2016.00645
Umair M, Sun N, Du H, Yuan J, Abbasi A, Wen J, Yu W, Zhou J, Liu C (2019) Differential metabolic responses of shrubs and grasses to water additions in arid karst region, southwestern China. Sci Rep 9:9613. https://doi.org/10.1038/s41598-019-46083-1
Umair M, Sun N, Du H, Chen K, Tao H, Yuan J, Abbasi A, Liu C (2020) Differential stoichiometric responses of shrubs and grasses to increased precipitation in a degraded karst ecosystem in southwestern China. Sci Total Environ 700:134421. https://doi.org/10.1016/j.scitotenv.2019.134421
Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozakia K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 41:17588–17593. https://doi.org/10.1073/pnas.0907095106
Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K et al (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839. https://doi.org/10.1093/pcp/pcq156
Van Breusegem F, Dat J (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390. https://doi.org/10.1104/pp.106.078295
Vlad F, Rubio S, Rodrigues A, Sirichandra C, Belin C, Robert N, Leung J, Rodriguez PL, Lauriere C, Merlot S (2009) Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21:3170–3184. https://doi.org/10.1105/tpc.109.069179
Vodnik D, Gričar J, Lavrič M, Ferlan M, Hafner P, Eler K (2019) Anatomical and physiological adjustments of pubescent oak (Quercus pubescens Willd.) from two adjacent sub-Mediterranean ecosites. Environ Exp Bot 165:208–218. https://doi.org/10.1016/j.envexpbot.2019.06.010
Vuralhan-Eckert J, Lautner S, Fromm J (2018) Effect of simultaneously induced environmental stimuli on electrical signalling and gas exchange in maize plants. J Plant Physiol 223:32–36. https://doi.org/10.1016/j.jplph.2018.02.003
Wang YJ, Yu JN, Chen T, Zhang ZG, Hao YJ, Zhang JS, Chen SY (2005) Functional analysis of a putative Ca2+ channel gene TaTPC1 from wheat. J Exp Bot 56:3051–3060. https://doi.org/10.1093/jxb/eri302
Wang X, Huang Y, Wang D, Lu S, Qin J (2009) Photosynthetic characteristics and chlorophyll fluorescence parameters of Pteroceltis tatarinowii in response to different habitats in karst area. For Res 22:475–481
Wang J, Wen X, Zhang X, Li S, Zhang D (2018a) Co-regulation of photosynthetic capacity by nitrogen, phosphorus and magnesium in a subtropical Karst forest in China. Sci Rep 8:7406. https://doi.org/10.1038/s41598-018-25839-1
Wang M, Chen H, Zhang W, Wang K (2018b) Soil nutrients and stoichiometric ratios as affected by land use and lithology at county scale in a karst area, southwest China. Sci Total Environ 619–620:1299–1307. https://doi.org/10.1016/j.scitotenv.2017.11.175
Wang K, Zhang C, Chen H, Yue Y, Zhang W, Zhang M, Qi X, Fu Z (2019) Karst landscapes of China: patterns, ecosystem processes and services. Landsc Ecol 34:2743–2763. https://doi.org/10.1007/s10980-019-00912-w
Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Freidit-Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1:198–217. https://doi.org/10.1093/mp/ssm022
Wei X, Deng X, Xiang W, Lei P, Ouyang S, Wen H, Chen L (2018) Calcium content and high calcium adaptation of plants in karst areas of southwestern Hunan, China. Biogeosciences 15:2991–3002. https://doi.org/10.5194/bg-15-2991-2018
Wu G, Li M, Zhong F, Fu C, Sun J, Yu L (2011) Lonicera confusa has an anatomical mechanism to respond to calcium-rich environment. Plant Soil 338:343–353. https://doi.org/10.1007/s11104-010-0549-1
Wu Q, Li Q, Li R, Zhou G (2018a) Study on the photosynthetic characteristics of two typical trees in the karst area of southern China. Fresenius Environ Bull 27:9066–9075
Wu Y, Hong W, Chen Y (2018b) Leaf physiological and anatomical characteristics of two indicator species in the limestone region of southern China under drought stress. Pak J Bot 50:1335–1342
Xiong L, Zhu J (2001) Abiotic stress signal transduction in plants: molecular and genetic perspectives. Physiol Plant 112:152–166. https://doi.org/10.1034/j.1399-3054.2001.1120202.x
Yan X, Cai Y (2013) Multi-scale anthropogenic driving forces of karst rocky desertification in Southwest China. Land Degrad Dev 26:193–200. https://doi.org/10.1002/ldr.2209
Yuan D (2001) On the karst ecosystem. Acta Geol Sin 75:336–338
Yudina L, Sukhova E, Sherstneva O, Grinberg M, Ladeynova M, Vodeneev V, Sukhov V (2020) Exogenous abscisic acid can influence photosynthetic processes in peas through a decrease in activity of H+-ATP-ase in the plasma membrane. Biology 9:324. https://doi.org/10.3390/biology9100324
Yue Y, Liao C, Tong X, Wu Z, Fensholt R, Prishchepov A, Jepsen M, Wang K, Brandt M (2020) Large scale reforestation of farmlands on sloping hills in South China karst. Landsc Ecol. https://doi.org/10.1007/s10980-020-01026-4
Zhang Z, Hu G, Ni J (2013) Effects of topographical and edaphic factors on the distribution of plant communities in two subtropical karst forests, southwestern China. J Mt Sci 10:95–104. https://doi.org/10.1007/s11629-013-2429-7
Zhang Z, Hu B, Hu G (2014) Spatial heterogeneity of soil chemical properties in a subtropical karst forest, Southwest China. Sci World J 2014:473651–473659. https://doi.org/10.1155/2014/473651
Zhang W, Zhao J, Pan F, Li D, Chen H, Wang K (2015) Changes in nitrogen and phosphorus limitation during secondary succession in a karst region in southwest China. Plant Soil 391:77–91. https://doi.org/10.1007/s11104-015-2406-8
Zhang J, Dai M, Wang L, Zeng C, Su W (2016) The challenge and future of rocky desertification control in karst areas in southwest China. Solid Earth 7:83–91. https://doi.org/10.5194/se-7-83-2016
Zhang XM, Liu LX, Gong JY, Tang J, Tang M, Yi Y (2017) Comparison of calcium distributions leaf cells of Carpinus pubescens and Camellia oleifera under drought and calcium stress. Pak J Bot 49:2139–2143
Zhang J, Wang J, Chen J, Song H, Li S, Zhao Y, Tao J, Liu J (2019) Soil moisture determines horizontal and vertical root extension in the perennial grass Lolium perenne L. growing in karst soil. Front Plant Sci 10:629. https://doi.org/10.3389/fpls.2019.00629
Zhao Y, Zou X, Gao J, Xu X, Wang C, Tang D, Wang T, Wu X (2015) Quantifying the anthropogenic and climatic contributions to changes in water discharge and sediment load into the sea: a case study of the Yangtze River, China. Sci Total Environ 536:803–812. https://doi.org/10.1016/j.scitotenv.2015.07.119
Zhu J (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324. https://doi.org/10.1016/j.cell.2016.08.029
Acknowledgements
This work was supported by the Guangxi science and technology base and talent project (Guike AD19245098); Guangxi Natural Science Foundation (2020GXNSFBA297045; 2020GXNSFBA297157); Research Project of Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection (ERESEP2020Z09); Sustainable development innovation project of Guangxi Normal University (2020CX003); Guangxi graduate education innovation program (YCSW2020104); Innovation training program for university students(202010602251).
Author information
Authors and Affiliations
Corresponding author
Additional information
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
Liu, C., Huang, Y., Wu, F. et al. Plant adaptability in karst regions. J Plant Res 134, 889–906 (2021). https://doi.org/10.1007/s10265-021-01330-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-021-01330-3