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Analysis of changes in anatomical characteristics and physiologic features of heteromorphic leaves in a desert tree, Populus euphratica

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Abstract

Populus euphratica Oliv. is well-adapted to extreme desert environments and possess the characteristic of heterophylly. On the same tree, the lanceolate, broad-ovate, and dentate broad-ovate leaves distribute in the different tiers of the canopy. The lanceolate leaves distribute on the lower canopy, broad-ovate leaves on the middle canopy, and dentate broad-ovate leaves on the upper canopy. The leaf structure was found to be xeromorphic. The stomatal densities of the three typical leaves were different and decreased in value from dentate broad-ovate, to broad-ovate, and to lanceolate leaves. The osmotic potentials at full and zero turgor were lowest in dentate broad-ovate leaves. In an appropriate growth environment, the chlorophyll fluorescence parameters of the three leaf types were almost the same and significantly changed upon exposure to short-term water stress. These results showed that dentate broad-ovate leaves can maintain their normal size and shape under arid and hot conditions because of their relatively thick cell wall and high mechanical strength. Moreover, dentate broad-ovate leaves had more developed vascular bundles in the main vein than the other types and thus more efficiently transported water and salts. These results suggested that dentate broad-ovate leaves can efficiently adapt to changing conditions, with more obvious xeromorphic characteristics and a relatively higher photosynthesis rate under drought conditions, compared with the others leaf types.

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Abbreviations

Ψ 100Л :

Osmotic potential at full turgor

Ψ 0Л :

Osmotic potential at turgor loss point

V a :

Apoplastic water fraction

ε :

Average modulus of elasticity

Chl a :

Chlorophyll a

Chl b :

Chlorophyll b

Chl (a + b):

Content of chlorophyll a + b

F 0 :

Minimum fluorescence of dark-adapted state

F m :

Maximum fluorescence of dark-adapted state

F v /F m :

Maximum quantum yield of PSII

References

  • Bai X, Zhang SJ, Zheng CX, Hao JQ, Li WH, Yang Y (2011) Comparative study on photosynthesis and water physiology of polymorphic leaves of Populus euphratica. J Beijing For Univ 33:47–52

    Google Scholar 

  • Bartlett MK, Scoffoni C, Sack L (2011) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15:393–405

    Article  Google Scholar 

  • Beckett RP (1997) Pressure-volume analysis of a range of poikilo hydric plants implies the existence of negative turgor in vegetative cells. Ann Bot 79:145–152

    Article  Google Scholar 

  • Chartzoulakis K, Patskas A, Kofidis G, Bosabalidis A, Nastou A (2002) Water stress affects leaf anatomy, gas exchange, water relations and growth of two avocado cultivers. Sci Hortic 95:39–50

    Article  CAS  Google Scholar 

  • Ding W, Yang ZH, Zhang SB, Chai SX (2010) Morphological and anatomical structure of leaves on Populus euphratica Oliv. in Qaidam basin. J Desert Res 30(6):1411–1415

    Google Scholar 

  • Dutta S, Mohanty S, Tripathy BC (2009) Role of temperature stress on chloroplast biogenesis and protein import in pea. Plant Physiol 150:1050–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • England JR, Attiwill PM (2006) Changes in leaf morphology and anatomy with tree age and height in the broad leaved evergreen species, Eucalyptus regnans F. Muell. Trees 20:79–90

    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 

  • Fu AH, Li WH, Chen YN, Zhu CG, Ma JX (2011) Analysis of dominant factors influencing moisture change of broad-ovate leaves of Populus euphratica Oliv. in extremely arid region. Photosynthetica 49:295–308

    Article  Google Scholar 

  • Gu RS, Liu QL, Pei D, Jiang XN (2004) Understanding saline and osmotic tolerance of Populus euphratica suspended cells. Plant Cell Tissue Organ Cult 78:261–265

    Article  CAS  Google Scholar 

  • Guo YH, Song XQ, Zhao ST, Lv JX, Lu MZ (2015) A transient gene expression system in Populous euphratica Oliv. protoplasts prepared from suspension cultured cells. Acta Physiol Plant 37:160. doi:10.1007/s11738-015-1906-8

    Article  Google Scholar 

  • Habermann G, Ellsworth PFV, Cazotoc JL, Simãoa E, Bierasa AC (2011) Comparative gas exchange performance during the wet season of three Brazilian Styrax species under habitat conditions of cerrado vegetation types differing in soil water availability and crown density. Flora 206:351–359

    Article  Google Scholar 

  • Hao JQ, Zhang L, Zheng CX, Bai X, Li WH (2011) Differences in chlorophyll fluorescence parameters and water content in heteromorphic leaves of Populus euphratica from Inner Mongolia. For Stud China 13:52–56

    Article  CAS  Google Scholar 

  • Hao JQ, Yue N, Zheng CX (2016) Selecting the optimum conditions for two dimensional difference gel electrophoresis of proteins expressed in Populus euphratica. Genet Mol Res. doi:10.4238/gmr.15028360

    Google Scholar 

  • Holbrook NM, Putz FE (1996) From epiphyte to tree: differences in leaf structure and leaf water relations associated with the transition in growth form in eight species of hemiepiphytes. Plant Cell Environ 19:631–642

    Article  Google Scholar 

  • Hukin D, Cochard H, Dreyer E, Thiec DL, Bogeat-Triboulot MB (2005) Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? J Exp Bot 56:2003–2010

    Article  CAS  PubMed  Google Scholar 

  • Li ZX, Zheng CX (2005) Structural characteristics and eco-adaptability of heteromorphic leaves of Populus euphratica. For Stud China 7(1):11–15

    Article  CAS  Google Scholar 

  • Li BS, Qin YR, Duan H, Yin WL, Xia XL (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XQ, Chang ZQ, Ma YL, Wu YX (2014) Characteristics of the fast chlorophyll fluorescence induction kinetics of heteromorphic leaves in Populus euphratica. J Desert Res 34(3):704–711

    Google Scholar 

  • Liu YB, Li XR, Chen GX, Li MM, Liu ML, Liu D (2015) Epidermal Micromophology and mesophyll structure of Populus euphratica heteromorphic leaves at different development stages. PLoS One. doi:10.1371/journal.pone.0137701

    Article  Google Scholar 

  • Lu YJ, Li NY, Sun J, Hou PC, Jing XS, Zhu HP, Deng SR, Han YS, Huang XX, Ma XJ, Zhao N, Zhang YH, Shen X, Chen SL (2013) Exogenous hydrogen peroxide, nitric oxide and calcium mediate root ion fluxes in two non-secretor mangrove species subjected to NaCl stress. Tree Physiol 33:81–95

    Article  PubMed  Google Scholar 

  • Luo L, Zhou WQ, Liu P, Li CX, Hou SW (2012) The development of stomata and other epidermal cells on the rice leaves. Biol Plant 56(3):521–527

    Article  Google Scholar 

  • Matthew OR, Rika JE (2012) Quantifying succulence: a rapid, physiologically meaningful metric of plant water storage. Plant Cell Environ 35:1533–1542

    Article  Google Scholar 

  • Mguis K, Albouchi A, Khadhri A, Abassi M, Yakoubi-Tej M, Mahjoub A, Ouerghi Z, Brahim NB (2012) Adjustments in leaf water relations of wild wheat relative Aegilops geniculata Roth. and wheat (Triticum durum Desf.) plants grown in a salinity gradient. AJCS 5:768–776

    Google Scholar 

  • Michelozzi M, Loreto F, Colom R, Rossi F, Calamassi R (2011) Drought responses in Aleppo pine seedlings from two wild provenances with different climatic features. Photosynthetica 49:564–572

    Article  CAS  Google Scholar 

  • Patakas A, Noitsakis B (1999) Osmotic adjustment and partitioning of turgor responses to drought in grapevines leaves. Am J Enol Vitic 50:76–80

    Google Scholar 

  • Perez-Martin A, Flexas J, Ribas-Carbó M, Bota J, Tomás M, Infante JM, Diaz-Espejo A (2009) Interactive effects of soil water deficit and air vapour pressure deficit on mesophyll conductance to CO2 in Vitis vinifera and Olea europaea. J Exp Bot 60:2391–2405

    Article  CAS  PubMed  Google Scholar 

  • Qiu J, Zheng CX, Yu WP (2005) Comparison of photosynthetic rate and fluorescence characteristics of heteromorphism leaf of Populus euphratica. Jilin For Sc Technols 34:19–21

    Google Scholar 

  • Qiu Q, Ma T, Hu QJ, Liu BB, Wu YX, Zhou HH, Wang Q, Wang J, Liu JQ (2011) Genome-scale transcriptome analysis of the desert poplar, Populus euphratica. Tree Physiol 31:452–461

    Article  PubMed  Google Scholar 

  • Sánchez-Blanco MJ, Morales MA, Torrecillas A, Alarcόn JJ (1998) Diurnal and seasonal osmotic potential changes in Lotus crestus plants grown under saline stress. Plant Sci 136:1–10

    Article  Google Scholar 

  • Sassi S, Aydi S, Hessini K, Gonzalez EM, Arrese-Igor C, Abdelly C (2010) Long-term mannitol-induced osmotic stress leads to stomatal closure, carbohydrate accumulation and changes in leaf elasticity in Phaselous vulgaris leaves. Afr J Biotechnol 9:6061–6069

    CAS  Google Scholar 

  • Silva P, Facanha AR, Tavares RM, Gerós H (2010) Role of tonoplast proton pumps and Na+/H+ antiport system in salt tolerance of Populus euphratica Oliv. J Plant Growth Regul 29:23–34

    Article  CAS  Google Scholar 

  • Su PX, Zhang LX, Du MW, Bi YR, Zhao AF, Liu XM (2003) Photosynthetic character and water use efficiency of different leaf shapes of Populus euphratica and their response to CO2 enrichment. Acta Phytoecol Sin 27:34–40

    Google Scholar 

  • Tan W, Hogan GD (1995) Effects of nitrogen limitations on water relations of jack pine (Pinus banksiana Lamb.) seedlings. Plant Cell Environ 18:757–764

    Article  CAS  Google Scholar 

  • Tyree MT, Hammel M (1972) The measurement of the turgor pressure and water relations of plants by the pressure-bomb technique. J Exp Bot 23:267–283

    Article  Google Scholar 

  • Vaz M, Cochard H, Gazarini L, Graca J, Chaves MM, Pereira JS (2012) Cork oak (Quercus suber L.) Seedlings acclimate to elevated CO2 and water stress: photosynthesis, growth, wood anatomy and hydraulic conductivity. Trees 26:1145–1157

    Article  CAS  Google Scholar 

  • Wang HL, Yang SD, Zhang CL (1997) The photosynthetic characteristics of differently shaped leaves in Populus euphratica Olivier. Photosynthetica 34:545–553

    Article  CAS  Google Scholar 

  • Wang HZ, Han L, Xu YL, Wang L, Jia WS (2011) Response of chlorophyll fluorescence characteristics of Populus euphratica heteromorphic leaves to high temperature. Acta Ecol Sin 31(9):2444–2453

    Google Scholar 

  • Wong SL, Chen CW, Huang HW, Weng JH (2012) Using combined measurements of gas exchange and chlorophyll fluorescence to investigate the photosynthetic light responses of plant species adapted to different light regimes. Photosynthetica 50:206–214

    Article  CAS  Google Scholar 

  • Xu Q, Chen YN (2012) Response of anatomy and hydraulic characteristics of xylem stem of Populus euphratica Oliv. to drought stress. Chin J Eco Agric 20:1059–1065

    Article  Google Scholar 

  • Yang SD, Zheng WJ, Chen GC, Zhang CL, Chen J, Wang XC (2005) Differences of ultrastructure and photosynthetic characteristics between lanceolate and broad-ovate leaves in Populus euphratica. Acta Bot Boreal Occident Sin 25(1):0014–0021

    CAS  Google Scholar 

  • Yu WL, Yang LL, Hu XL (2009) Drought tolerance characteristics of Populus euphratica narrow leaf and broad leaf at different ages in Ejina. J Inner Mong For Sci Technol 359(4):6–11

    Google Scholar 

  • Yue N, Zheng CX, Bai X, Hao JQ (2009) Proteomics analysis of heteromorphic leaves of Populus euphratica Oliv. China Biotechnol 29:40–44

    CAS  Google Scholar 

  • Zai XM, Zhu SN, Qin P, Wang XY, Che L, Luo FX (2012) Effect of Glomus mosseae on chlorophyll content, chlorophyll fluorescence parameters, and chloroplast ultrastructure of beach plum (Prunus maritima) under NaCl stress. Photosynthetica 50:323–328

    Article  CAS  Google Scholar 

  • Zhang XR, Wu H, Hu ZH (1997) Relationship between morphology and structure of leaves of the main sand-fixed plants in Mao US desert and environment. Acta Bot Boreal Occident Sin 17:54–60

    Google Scholar 

  • Zheng CX, Qiu J, Jiang CN, Yue N, Wang XQ, Wang WF (2007) Comparion of characteristics of stomas and photosynthesis of Populus euphratica polymorphic leaves. Front For China 2:87–93

    Article  Google Scholar 

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Acknowledgements

Funding as provided by the National Natural Science Foundation of China (Grant No. 30671655).

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Correspondence to Caixia Zheng.

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Communicated by B Zheng.

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Hao, J., Yue, N. & Zheng, C. Analysis of changes in anatomical characteristics and physiologic features of heteromorphic leaves in a desert tree, Populus euphratica . Acta Physiol Plant 39, 160 (2017). https://doi.org/10.1007/s11738-017-2467-9

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  • DOI: https://doi.org/10.1007/s11738-017-2467-9

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