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Photosynthetic and ultrastructural adaptability of Anemone shikokiana leaves to heterogeneous habitats

  • Ecology & Biogeography - Original Article
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Abstract

Anemone shikokiana (Makina) Makina is distributed in two heterogeneous habitats, including mountaintop shrubland and conifer and broad-leaf mixed forest. To better understand the mechanisms used by A. shikokiana in adapting to these different environments, the photosynthetic efficiency, chlorophyll fluorescence and ultrastructure of the leaves were investigated. The findings revealed that, under the same optical quantum flux density, the net photosynthetic rate in the leaves of mountaintop shrubland was significantly higher than that found in the mixed forest, but the stomatal conductance, intercellular CO2 concentrations and transpiration rate were lower. The effective quantum yield of photosystem II (PSII), photochemical quenching coefficient, non-photochemical quenching coefficient and electron transfer rate in the conifer and broad-leaf mixed forest were significantly lower than those values determined for plants in mountaintop shrubland. However, the maximal quantum yield of PSII exhibited no significant difference between the two habitats. Transmission electron micrographs revealed that the numbers of chloroplasts and mitochondria per mesophyll cell and starch grains per chloroplast in the mountaintop shrubs were higher than those found in the conifer and broad-leaf mixed forest samples. Moreover, they showed an increasing trend month by month in April, May and June. It indicated that elevated temperature increased their numbers. These findings illustrate that A. shikokiana efficiently uses environmentally limited resources to adapt to different living environments. The study reveals that the mechanisms that underlie the response of A. shikokiana to heterogeneous habitats involve photosynthetic and ultrastructural variations, thus providing a theoretical basis for future study.

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References

  • Alamin Md, Zeng DD, Sultana MH, Qin R, Jin XL, Shi CH (2018) Photosynthesis, cellulose contents and ultrastructure changes of mutant rice leading to screw flag leaf. Plant Growth Regul. https://doi.org/10.1007/s10725-018-0369-5

    Article  Google Scholar 

  • Alkhatib R, Alkhatib B, Al-Eitan L, Abdo N, Tadros M, Bsoul E (2018) Physio-anatomical responses of tobacco under caffeine stress. Photosynthetica 56:1140–1146

    Article  CAS  Google Scholar 

  • Almeida JD, Herrera A, Tezara W (2018) Phenotypic plasticity to photon flux density of physiological, anatomical and growth traits in a modern Criollo cocoa clone. Physiol Plant. https://doi.org/10.1111/ppl.12840

    Article  Google Scholar 

  • Bian FH, Pang YJ, Wang Z, Liu CL (2015a) Genetic diversity of Anemone shikokiana (Makino) Makino analyzed using the proteomics-based approach. Curr Proteom 12:4–13

    Article  CAS  Google Scholar 

  • Bian FH, Pang YJ, Wang Z, Liu CL, Zhuang SH (2015b) Genetic diversity of the rare plant Anemone shikokiana (Makino) Makino (Ranunculaceae) inferred from AFLP markers. Plant Syst Evol 301:677–684

    Article  Google Scholar 

  • Bian FH, Chen P, Yu WY (2018) Breeding system of Anemone shikokiana and the influential factors of fruit-setting ratio in different habitats. Plant Biosyst 152:445–452

    Article  Google Scholar 

  • Chapin FS III (1987) Environmental controls over growth of tundra plants. Ecol Bull 38:69–76

    Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought-from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Čiamporová M (1987) The development of structural changes in epidermal ceils of maize roots during water stress. Biol Plant 29:290–294

    Article  Google Scholar 

  • Čiamporová M, Mistrík I (1993) The impact of the environment on roots and root systems the ultrastructural response of root cells to stressful conditions. Environ Exp Bot 33:11–26

    Article  Google Scholar 

  • Djanaguiraman M, Prasad PV, Boyle D, Schapaugh W (2011) Hightemperature stress and soybean leaves: leaf anatomy and photosynthesis. Crop Sci 51:2125–2131

    Article  Google Scholar 

  • Eckard G (1979) Sun and shade ecotypes of Solanum dulcamara l.: photosynthetic light dependence characteristics in relation to mild water stress. Oecologia (Berlin) 39:61–70

    Article  Google Scholar 

  • Ennajeh M, Vadel AM, Cochard H, Khemira H (2010) Comparative impacts of water stress on the leaf anatomy of a drought-resistant and a drought-sensitive olive cultivar. J Hortic Sci Biotechnol 85:289–294

    Article  Google Scholar 

  • Ferguson J, Humphry M, Lawson T, Brendel O, Bechtold U (2018) Natural variation of life-history traits, water use, and drought responses in Arabidopsis. Plant Direct 2:1–16

    Article  CAS  Google Scholar 

  • Figueiredo-Lima KV, Falcão HM, Melo-de-Pinna GF, Albacete A, Dodd IC, Lima AL, Santos MG (2018) Leaf phytohormone levels and stomatal control in an evergreen woody species under semiarid environment in a Brazilian seasonally dry tropical forest. Plant Growth Regul 85:437–445

    Article  CAS  Google Scholar 

  • Gao HY, Li JW, Ji HN, An LJ, Xia XY (2018) Hyperhydricity-induced ultrastructural and physiological changes in blueberry (Vaccinium spp.). Plant Cell Tissue Org 133:65–76

    Article  CAS  Google Scholar 

  • Gao S, Liu XN, Liu Y, Cao BL, Chen ZJ, Xu K (2020) Photosynthetic characteristics and chloroplast ultrastructure of welsh onion (Allium fistulosum L.) grown under different LED wavelengths. BMC Plant Biol 20:78

    Article  CAS  Google Scholar 

  • Gonzalez-Paleo L, Ravetta D (2018) Relationship between photosynthetic rate, water use and leaf structure in desert annual and perennial forbs differing in their growth. Photosynthetica 56:1177–1187

    Article  CAS  Google Scholar 

  • Griffin JJ, Ranney TG, Pharr DM (2004) Photosynthesis, chlorophyll fluorescence, and carbohydrate content of Illicium taxa grown under varied irradiance. J Am Soc Horticult Sci 1:46–53

    Article  Google Scholar 

  • Guo S, Zhou Y, Shen Q, Zhang F (2007) Effect of ammonium and nitrate nutrition on some physiological processes in higher plants growth, photosynthesis, photorespiration, and water relations. Plant Biol 9:21–29

    Article  CAS  Google Scholar 

  • Gupta SK, Prakash J, Srivastava S (2002) Validation of claim of Tulsi, Ocimum sanctum L. as a medicinal plant. Indian J Exp Biol 40:765–773

    CAS  Google Scholar 

  • Haffani S, Mezni M, Nasri MB, Chaibi W (2017) Comparative leaf water relations and anatomical responses of three vetch species (Vicia narbonensis L., V. sativa L. and V. villosa Roth.) to cope with water stress. Crop Pasture Sci 68:691–702

    Article  Google Scholar 

  • Han JM, Lei ZY, Zhang YJ, Yi XP, Zhang WF, Zhang YL (2018) Drought introduced variability of mesophyll conductance in Gossypium and its relationship with leaf anatomy. Physiol Plant. https://doi.org/10.1111/ppl.12845

    Article  Google Scholar 

  • Herritt MT, Fritschi FB (2020) Characterization of photosynthetic phenotypes and chloroplast ultrastructural changes of soybean (Glycine max) in response to elevated air temperatures. Front Plant Sci 11:153

    Article  Google Scholar 

  • Heschel M, Sultan S, Glover SD (2004) Population differentiation and plastic responses to drought stress in the generalist annual Polygonum persicaria. Int J Plant Sci 165:817–824

    Article  Google Scholar 

  • Jenny A, Mark W, Robin G, Caroline A, Alexander V, Peter H et al (2003) Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II—effects on photosynthesis, grana stacking and fitness. Plant J 35:350–361

    Article  CAS  Google Scholar 

  • Jia W, Zhang J (2008) Stomatal movements and long-distance signaling in plants. Plant Signal Behav 3:772–777

    Article  Google Scholar 

  • Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A et al (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res 132:13–66

    Article  CAS  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. In: Levitt J (ed) Chilling, freezing, and high temperature stresses, 2nd edn. Academic Press, New York, pp 497–607

    Google Scholar 

  • Lichtenthaler HK, Babani F, Langsdorf G (2007) Chlorophyll fluorescence imaging of photosynthetic activity in sun and shade leaves of trees. Photosynth Res 93:235

    Article  CAS  Google Scholar 

  • Lima Neto MC, Lobo Ana KM, Martins MO, Fontenele AV, Silveira JAG (2014) Dissipation of excess photosynthetic energy contributes to salinity tolerance: a comparative study of salt-tolerant Ricinus communis and salt-sensitive Jatropha curcas. J Plant Physiol 171:23–30

    Article  CAS  Google Scholar 

  • Liu BB, Li M, Li QM, Cui QQ, Zhang WD, Ai XZ, Bi HG (2018a) Combined effects of elevated CO2 concentration and drought stress on photosynthetic performance and leaf structure of cucumber (Cucumis sativus L.) seedlings. Photosynthetica 56:942–952

    Article  CAS  Google Scholar 

  • Liu XY, Jiao XL, Chang TT, Guo SR, Xu ZG (2018b) Photosynthesis and leaf development of cherry tomato seedlings under different LED-based blue and red photon flux ratios. Photosynthetica. https://doi.org/10.1007/s11099-018-0814-8

    Article  Google Scholar 

  • Lu YW, Miao XL, Song QY, Peng SM, Duan BL (2018) Morphological and ecophysiological plasticity in dioecious plant Populus tomentosa under drought and alkaline stresses. Photosynthetica 56:1353–1364

    Article  CAS  Google Scholar 

  • Malinowski R (2013) Understanding of leaf development-the science of complexity. Plants (Basel) 2:396–415

    Article  CAS  Google Scholar 

  • Mathur S, Kalaji HM, Jajoo A (2016) Investigation of deleterious effects of chromium phytotoxicity and photosynthesis in wheat plant. Photosynthetica 54:185–192

    Article  CAS  Google Scholar 

  • Matos FS, Wolfgramm R, Gonçalves FV, Cavatte P, Ventrella M, DaMatta FM (2009) Phenotypic plasticity in response to light in the coffee tree. Environ Exp Bot 67:421–427

    Article  CAS  Google Scholar 

  • Montgomery RA, Givnish TG (2008) Adaptive radiation of photosynthetic physiology in the Hawaiian lobeliads: dynamic photosynthetic responses. Oecologia 155:455–467

    Article  Google Scholar 

  • Mudrik V, Kosobrukhov A, Knyazeva I, Pigulevskaya T (2003) Changes in the photosynthetic characteristics of Plantago major plants caused by soil drought stress. Plant Growth Regul 40:1–6

    Article  CAS  Google Scholar 

  • Nadal M, Flexas J (2018) Mesophyll conductance to CO2 diffusion of drought and opportunities for improvement. In: García-Tejero IF, Durán-Zuazo VH (eds) Water scarcity and sustainable agriculture in semiarid environment: tools, strategies and challenges for woody crops. Academic Press, New York, pp 403–438

    Chapter  Google Scholar 

  • Ohsumi A, Hamasaki A, Nakagawa H, Yoshida H, Shiraiwa T, Horie T (2007) A model explaining genotypic and ontogenetic variation of leaf photosynthetic rate in rice (Oryza sativa) based on leaf nitrogen content and stomatal conductance. Ann Bot 99:265–273

    Article  CAS  Google Scholar 

  • Romero-Munar A, Baraza E, Cifre J, Achir C, Gulías J (2018) Leaf plasticity and stomatal regulation determines the ability of Arundo donax plantlets to cope with water stress. Photosynthetica 56:698–706

    Article  Google Scholar 

  • Sahoo MR, Dasgupta M, Pc Kole, Mukherjee A (2018) Photosynthetic, physiological and biochemical events associated with polyethylene glycol-mediated osmotic stress tolerance in taro (Colocasia esculenta L. Schott). Photosynthetica 56:1069–1080

    Article  CAS  Google Scholar 

  • Shan L, Xu BC (2009) Discussion on establishing stable artificial grassland in semiarid region on Loess Plateau. Acta Pratac Sin 18:1–2

    Google Scholar 

  • Shao RX, Xin LF, Guo JM, Zheng HF, Mao J, Han XP, Jia L, Jia SJ, Du CG, Song R, Yang QH, Elmore RW (2018) Salicylic acid-induced photosynthetic adaptability of Zea mays L. to polyethylene glycol-simulated water deficit is associated with nitric oxide signaling. Photosynthetica 56:1370–1377

    Article  CAS  Google Scholar 

  • Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040

    Article  CAS  Google Scholar 

  • Sikder S, Foulkes J, West H, Silva JD, Gaju O, Greenland A, Howell P (2015) Evaluation of photosynthetic potential of wheat genotypes under drought condition. Photosynthetica 53:47–54

    Article  CAS  Google Scholar 

  • Sun AZ, Guo FQ (2016) Chloroplast retrograde regulation of heat stress responses in plants. Front Plant Sci 7:398

    Google Scholar 

  • Tang Y, Wen X, Lu Q, Yang Z, Cheng Z, Lu C (2007) Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants. Plant Physiol 143:629–638

    Article  CAS  Google Scholar 

  • Teng S, Qian Q, Zeng DL, Yasufumi K, Hiroshi F, Huang DN, Zhu LH (2002) QTL analysis of leaf photosynthetic rate and related physiological traits in rice (Oryza sativa L.). Chin Rice Res Newsl 10:1–7

    Google Scholar 

  • Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A (2015) Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep 5:12449

    Article  Google Scholar 

  • Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Ann Rev Ecol Evol Syst 38:237–257

    Article  Google Scholar 

  • Vani B, Saradhi PP, Mohanty P (2001) Alteration in chloroplast structure and thylakoid membrane composition due to in vivo heat treatment of rice seedlings: correlation with the functional changes. J Plant Physiol 158:583–592

    Article  CAS  Google Scholar 

  • Vartapetian BB, Andreeva IN, Generozova IP, Polyakova LI, Maslova IP, Dolgikh YI, Stepanova AY (2003) Functional electron microscopy in studies of plant response and adaptation to anaerobic stress. Ann Bot 9:155–172

    Article  CAS  Google Scholar 

  • Vassileva V, Demirevska K, Simova-Stoilova L, Petrova T, Tsenov N, Feller U (2012) Long-term field drought affects leaf protein pattern and chloroplast ultrastructure of winter wheat in a cultivar-specific manner. J Agron Crop Sci 198:104–117

    Article  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    Article  CAS  Google Scholar 

  • Xu S, Li JL, Zhang XQ, Wei H, Cui LJ (2006) Effectsofheatacclimation pretreatment on changes ofmembrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56:274–285

    Article  CAS  Google Scholar 

  • Xu WZ, Deng XP, Xu BC (2013) Effects of water stress and fertilization on leaf gas exchange and photosynthetic light-response curves of Bothriochloa ischaemum L. Photosynthetica 51:603–612

    Article  CAS  Google Scholar 

  • Yang XY, Jiang B, Feng L, Gao Y, Bian FH (2019) Optimization of light-response curves and analysis of photosynthetic physiological characteristic of Anemone shikokiana in heterogeneous habitats. Heilongjiang Agric Sci 7:12–17

    Google Scholar 

  • Yu WY, Gao Y, Pang YJ, Wang Z, Bian FH (2019) Response of leaf morphology and structure of Anemone shikokiana to heterogeneous habitats and altitude changes. Acta Ecol Sin 39:4413–4420

    Google Scholar 

  • Zhang R, Wise RR, Struck KR, Sharkey TD (2010) Moderate heat stress of Arabidopsis thaliana leaves causes chloroplast swelling and plastoglobule formation. Photosynth Res 105:123–134

    Article  CAS  Google Scholar 

  • Zhang FJ, Zhang KK, Du CZ, Li J, Xing YX, Yang LT, Li YR (2015) Effect of drought stress on anatomical structure and chloroplast ultrastructure in leaves of sugarcane. Sugar Technol 17:41–48

    Article  Google Scholar 

  • Zhou X, Zhu T, Zhu LS, Luo SS, Deng XG, Lin HH, Xi DH (2017) The role of photoreceptors in response to cucumber mosaic virus in Arabidopsis thaliana. J Plant Growth Regul 36:257–270

    Article  CAS  Google Scholar 

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Acknowledgements

This study was funded by the Natural Science Foundation of Shandong Province (Grant No. ZR2018MC003) and National Natural Science Foundation of China (Grant No. 31971546).

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FB supervised the study; YP collected the data, made the photographs and wrote the manuscript; LL performed the analyses of data. Three authors approved the final version of the manuscript.

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Correspondence to Fuhua Bian.

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Pang, Y., Li, L. & Bian, F. Photosynthetic and ultrastructural adaptability of Anemone shikokiana leaves to heterogeneous habitats. Braz. J. Bot 43, 979–988 (2020). https://doi.org/10.1007/s40415-020-00645-0

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