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Anatomy and transcriptome analysis in leaves revealed how nitrogen (N) availability influence drought acclimation of Populus

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The expression of drought responsive genes were enhanced by N application and they contributed to drought acclimation.

Abstract

The interactive effects of water and nutrient are crucial for plants. The aim of this study was to elucidate how nitrogen (N) status influence drought acclimation of Populus. A two-factorial design consisting of two N levels (adequate-N and low-N) and two watering treatments (drought stress and well-watered) was used, and an integrative investigation was conducted at the anatomical, physiological and molecular levels. Adequate N supply alleviated the adverse effects of drought stress on root growth in poplars, which may increase water uptake under drought. Nitrogen enhanced leaf anatomical changes and stomata adjustment upon drought stress, lead to less water losses and better growth performance under drought stress. The expression levels of phytohormone signaling components and genes responsible for antioxidative systems and secondary metabolites such as phenylpropanoids were promoted by N application. The expression of abscisic acid (ABA) signaling components was induced by drought when soil N was adequate, which participated in stomata regulation and drought acclimation. The expression of indole acetic acid (IAA) signaling components also was enhanced by N application, which participated in anatomical changes of leaves under drought. These adaptive changes at molecular and anatomical levels contributed to drought acclimation in a synergistic way. Under adequate-N condition, nitrogen and carbon metabolism pathways are being recruited to combat drought, and the C-N interaction play a pivotal role in drought acclimation.

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References

  • Beniwal RS, Langenfeld-Heyser R, Polle A (2010) Ectomycorrhiza and hydrogel protect hybrid poplar from water deficit and unravel plastic responses of xylem anatomy. Environ Exp Bot 69:189–197

    Article  Google Scholar 

  • Cao X, Jia J, Li H, Li M, Luo J, Liang Z, Luo ZB (2012) Photosynthesis, water use efficiency and stable carbon isotope composition are associated with anatomical properties of leaf and xylem in six poplar species. Plant Biol 14:612–620

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Jia J, Zhang C, Li H, Liu T, Jiang X, Luo ZB (2014) Anatomical, physiological and transcriptional responses of two contrasting poplar genotypes to drought and re-watering. Physiol Plantarum 151:480–494

    Article  CAS  Google Scholar 

  • Cho YH, Yoo SD, Sheen J (2006) Regulatory functions of nuclear hexokinase 1 complex in glucose signaling. Cell 127:579–589

    Article  CAS  PubMed  Google Scholar 

  • Comas LH, Becker SR, Cruz VMV, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding L, Gao CM, Li YR, Li YR, Li Y, Zhu YY, Xu GH, Shen QR, Kaldenhof R, Kai L, Guo SW (2015) The enhanced drought tolerance of rice plants under ammonium is related to aquaporin (AQP). Plant Sci 234:14–21

    Article  CAS  PubMed  Google Scholar 

  • Du H, Wu N, Chang Y, Li XH, Xiao JH, Xiong LZ (2013) Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Mol Biol 83:475–488

    Article  CAS  Google Scholar 

  • Dziedek C, Oheimb G, Calvo L, Fichtner A, Kriebitzsch WU, Marcos E, Pitz WT, Hardtle W (2016) Does excess nitrogen supply increase the drought sensitivity of European beech (Fagus sylvatica L.) seedlings? Plant Ecol 217:393–405

    Article  Google Scholar 

  • Fritz C, Palacios-Rojas N, Feil R, Stitt M (2006) Regulation of secondary metabolism by the carbon–nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J 46:533–548

    Article  CAS  PubMed  Google Scholar 

  • Gan HH, Jiao Y, Jia J, Wang X, Li H, Shi W, Peng C, Polle A, Luo ZB (2016) Phosphorus and nitrogen physiology of two contrasting poplar genotypes when exposed to phosphorus and/or nitrogen starvation. Tree Physiol 36(1):22–38

    Article  CAS  PubMed  Google Scholar 

  • Gessler A, Schaub M, McDowell NG (2017) The role of nutrients in drought-induced tree mortality and recovery. New Phytol 214:513–520

    Article  CAS  PubMed  Google Scholar 

  • He MZ, Dijkstra FA (2014) Drought effect on plant nitrogen and phosphorus: a meta analysis. New Phytol 204:924–931

    Article  CAS  PubMed  Google Scholar 

  • Honda MDH, Ishihara KL, Pham DT, Borthakur D (2018) Identification of drought-induced genes in giant leucaena (Leucaena leucocephala subsp. glabrata). Trees 32:571

    Article  CAS  Google Scholar 

  • Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162

    Article  PubMed  Google Scholar 

  • Jing DL, Xia Y, Chen F, Wang Z, Zhang SG, Wang JH (2015) Ectopic expression of a Catalpa bungei (Bignoniaceae) PISTILLATA homologue rescues the petal and stamen identities in Arabidopsis pi-1 mutant. Plant Sci 231:40–51

    Article  CAS  PubMed  Google Scholar 

  • Li H, Li M, Luo J, Cao X, Qu L, Gai Y, Jiang XN, Liu TX, Bai H, Janz D, Polle A, Peng CH, Luo ZB (2012) N-fertilization has different effects on the growth, carbon and nitrogen physiology, and wood properties of slow- and fast-growing Populus species. J Exp Bot 63(2):695–709

    Article  CAS  Google Scholar 

  • Li Q, Lei S, Du K, Li LZ, Pang XF, Wang ZC, Wei M, Fu S, Hu LM, Xu L (2016) RNA-seq based transcriptomic analysis uncovers α-linolenic acid and jasmonic acid biosynthesis pathways respond to cold acclimation in Camellia japonica. Sci Rep-UK 6:36463. https://doi.org/10.1038/srep36463

    Article  CAS  Google Scholar 

  • Li H, Li M, Wei XL, Zhang X, Xue R, Zhao YD, Zhao HJ (2017) Transcriptome analysis of drought–responsive genes regulated by hydrogen sulfide in wheat (Triticum aestivum L.) leaves. Mol Genet Genomics 292:1091–1110

    Article  CAS  PubMed  Google Scholar 

  • Luo ZB, Li K, Jiang X, Polle A (2009) Ectomycorrhizal fungus (Paxillus involutus) and hydrogels affect performance of Populus euphratica exposed to drought stress. Ann Forest Sci 66:106

    Article  CAS  Google Scholar 

  • Luo J, Li H, Liu TX, Polle A, Peng CH, Luo ZB (2013) Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. J Exp Bot 64:4207–4224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo J, Zhou J, Li H, Shi WG, Polle A, Lu MZ, Sun XM, Luo ZB (2015) Global poplar root and leaf transcriptomes reveal links between growth and stress responses under nitrogen starvation and excess. Tree Physiol 35:1283–1302

    Article  CAS  PubMed  Google Scholar 

  • Meng S, Zhang C, Su L, Li Y, Zhao Z (2016) Nitrogen uptake and metabolism of Populus simonii in response to PEG-induced drought stress. Environ Exp Bot 123:78–87

    Article  CAS  Google Scholar 

  • Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3:973–996

    Article  CAS  PubMed  Google Scholar 

  • Qiu T, Chen Y, Li M, Kong Y, Zhu Y, Han N, Bian H, Zhu M, Wang JH (2013) The tissue-specific and developmentally regulated expression patterns of the SAUR41 subfamily of SMALL AUXIN UP RNA genes. Plant Signal Behav 8(e25283):8. https://doi.org/10.4161/psb.25283

    Article  CAS  Google Scholar 

  • Roggatz U, Mcdonald AJS, Stadenberg I, Schurr U (1999) Effects of nitrogen deprivation on cell division and expansion in leaves of Ricinus communis L. Plant Cell Environ 22(1):81–89

    Article  Google Scholar 

  • Savoi S, Wong DCJ, Arapitsas P, Mara M, Bucchetti B, Peterlunger E, Fait A, Mattivi F, Castellarin SD (2016) Transcriptome and metabolite profiling reveals that prolonged drought modulates the phenylpropanoid and terpenoid pathway in white grapes (Vitis vinifera L.). BMC Plant Biol 16:67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi WG, Li H, Liu TX, Polle A, Peng CH, Luo ZB (2015) Exogenous abscisic acid alleviates zinc uptake and accumulation in Populus × canescens exposed to excess zinc. Plant Cell Environ 38:207–223

    Article  CAS  PubMed  Google Scholar 

  • Shi HL, Ma WJ, Song JY, Lu M, Rahman SU, Bui TTX, Vu DD, Zheng HF, Wang JH, Zhang Y (2017) Physiological and transcriptional responses of Catalpa bungei to drought stress under sufficient- and deficient-nitrogen conditions. Tree Physiol 37:1457–1468

    Article  CAS  PubMed  Google Scholar 

  • Shimshi D (1970) The effect of nitrogen supply on transpiration and stomatal behaviour of beans (Phaseolus vulgaris L.). New Phytol 69(2):405–412

    Article  Google Scholar 

  • Singh AK, Elvitigala T, Bhattacharyya-Pakrasi M, Aurora R, Ghosh B, Pakrasi HB (2008) Integration of carbon and nitrogen metabolism with energy production is crucial to light acclimation in the Cyano bacterium Synechocystis. Plant Physiol 148:467–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soon FF, Ng LM, Zhou XE, West GM, Kovach A, Tan MHE, Suino-Powell KM, He YZ, Xu Y, Chalmers MJ, Brunzelle JS, Zhang HM, Yang HY, Jiang HL, Li J, Yong EL, Cutler S, Zhu JK, Griffin PR, Melcher K, Xu HE (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335:85–88

    Article  CAS  PubMed  Google Scholar 

  • Sorin C, Leport L, Mireille Cambert M, Bouchereau A, Mariette F, Musse M (2016) Nitrogen deficiency impacts on leaf cell and tissue structure with consequences for senescence associated processes in Brassica napus. Bot Study 57:11

    Article  CAS  Google Scholar 

  • Steinemann S, Zeng ZH, McKay A, Heuer S, Langridge P, Huang CY (2015) Dynamic root responses to drought and re-watering in two wheat (Triticum aestivum) genotypes. Plant Soil 391:139–152

    Article  CAS  Google Scholar 

  • Tran TT, Kano-Nakata M, Takeda M, Menge D, Mitsuya S, Inukai Y, Yamauchi A (2014) Nitrogen application enhanced the expression of developmental plasticity of root systems triggered by mild drought stress in rice. Plant Soil 378:139–152

    Article  CAS  Google Scholar 

  • Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Ruan LL (2013) Regulation of cell division and expansion by sugar and auxin signaling. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00163

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang P, Ma LL, Li Y, Wang SA, Li LF, Yang RT, Ma YZ, Wang Q (2016) Transcriptome profiling of indole-3-butyric acid-induced adventitious root formation in softwood cuttings of the Catalpa bungei variety ‘YU-1’ at different developmental stages. Genes Genom 38:145–162

    Article  CAS  Google Scholar 

  • Wang ZQ, Gu CS, Xuan L, Hua JF, Shi Q, Fan WC, Yin YL, Yu FY (2017) Identification of suitable reference genes in Taxodium ‘Zhongshanshan’ under abiotic stresses. Trees 31:1519–1530

    Article  CAS  Google Scholar 

  • Xu N, Guo W, Liu J, Du N, Wang R (2015) Increased nitrogen deposition alleviated the adverse effects of drought stress on Quercus variabilis and Quercus mongolica seedlings. Acta Physiol Plant 37:107

    Article  CAS  Google Scholar 

  • Yang Y, Guo JY, Wang GX, Yang LD, Yang Y (2012) Effects of drought and nitrogen addition on photosynthetic characteristics and resource allocation of Abies fabri seedlings in eastern Tibetan Plateau. New For 43:505–518

    Article  Google Scholar 

  • Zhang Y, Zhou ZC, Yang Q (2013) Genetic variations in root morphology and phosphorus efficiency of Pinus massoniana under heterogeneous and homogeneous low phosphorus conditions. Plant Soil 364:93–104

    Article  CAS  Google Scholar 

  • Zheng HF, Zhang X, Ma WJ, Song JY, Rahman S, Wang JH, Zhang Y (2017) Morphological and physiological responses to cyclic drought in two contrasting genotypes of Catalpa bungei. Environ Exp Bot 138:77–87

    Article  Google Scholar 

Download references

Acknowledgements

This research was financially supported by National Key R&D Program of China (Grant No. 2016YFD0600105), the Start-up Project for Introduced Recruit in Northwest A&F University (No. Z111021402), and the Fundamental Research Funds for the Central Universities (No. 2452016056). For the technical assistance in dataset analysis, we would like to thank Biobreeding Biotechnology Corporation (Shaanxi, China).

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Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology in Arid Areas, College of Forestry, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Mei Lu, Mengmeng Chen, Junyu Song, Yang Wang, Yuehan Pan, Chunyan Wang, Junfeng Fan & Yi Zhang

  2. The UWA Institute of Agriculture, The University of Western Australia, Perth, WA, 6001, Australia

    Jiayin Pang

  3. School of Biological Science, The University of Western Australia, Perth, WA, 6001, Australia

    Yi Zhang

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  1. Mei Lu
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Correspondence to Chunyan Wang or Yi Zhang.

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Lu, M., Chen, M., Song, J. et al. Anatomy and transcriptome analysis in leaves revealed how nitrogen (N) availability influence drought acclimation of Populus. Trees 33, 1003–1014 (2019). https://doi.org/10.1007/s00468-019-01834-5

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