|
Special Issue:
玉米遗传育种合辑Maize Genetics · Breeding · Germplasm Resources
|
|
|
|
| Metabolic responses to combined water deficit and salt stress in maize primary roots |
LI Peng-cheng1, 2*, YANG Xiao-yi1*, WANG Hou-miao1, 2, PAN Ting1, YANG Ji-yuan1, WANG Yun-yun1, XU Yang1, 2, YANG Ze-feng1, 2, 3, XU Chen-wu1, 2, 3 |
1 Jiangsu Key Laboratory of Crop Genetics and Physiology/Key Laboratory of Plant Functional Genomics, Ministry of Education/Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/Agricultural College, Yangzhou University, Yangzhou 225009, P.R.China
2 Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, P.R.China
3 Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education/Yangzhou University, Yangzhou 225009, P.R.China |
|
|
|
|
摘要
土壤干旱和盐胁迫是植物生长和农业生产力的主要限制因素。主胚根是感知干旱和盐分胁迫信号的第一个器官。研究发现，与对照植株相比，遭受干旱、高盐和复合胁迫的玉米植株的主胚根长度明显变短。利用气相色谱-质谱联用技术测定了玉米主胚根在干旱、高盐和复合胁迫下代谢产物的变化。本研究共测定86种代谢产物，包括29种氨基酸和胺，21种有机酸，4种脂肪酸，6种磷酸，10种多糖，10种多元醇和6种其他代谢物。其中，53个代谢物在不同胁迫下均有显著变化，且大部分代谢物含量呈下降趋势。共计4种和18种代谢物分别对三种处理均有显著的上调和下调。糖和多元醇等可溶性物质的含量增加以维持渗透平衡。TCA循环中柠檬酸、酮戊二酸、延胡索酸、苹果酸的水平显著降低，莽草酸途径中奎宁酸、莽草酸等代谢物含量显著降低。本研究揭示了主胚根在干旱和盐胁迫复合作用下的复杂代谢反应，拓展了我们对玉米根系对非生物耐受性反应机制的理解。
Abstract Soil water deficit and salt stress are major limiting factors of plant growth and agricultural productivity. The primary root is the first organ to perceive the stress signals for drought and salt stress. In this study, maize plant subjected to drought, salt and combined stresses displayed a significantly reduced primary root length relative to the control plants. GC-MS was used to determine changes in the metabolites of the primary root of maize in response to salt, drought and combined stresses. A total of 86 metabolites were measured, including 29 amino acids and amines, 21 organic acids, four fatty acids, six phosphoric acids, 10 sugars, 10 polyols, and six others. Among these, 53 metabolites with a significant change under different stresses were identified in the primary root, and the content of most metabolites showed down-accumulation. A total of four and 18 metabolites showed significant up- and down-accumulation to all three treatments, respectively. The levels of several compatible solutes, including sugars and polyols, were increased to help maintain the osmotic balance. The levels of metabolites involved in the TCA cycle, including citric acid, ketoglutaric acid, fumaric acid, and malic acid, were reduced in the primary root. The contents of metabolites in the shikimate pathway, such as quinic acid and shikimic acid, were significantly decreased. This study reveals the complex metabolic responses of the primary root to combined drought and salt stresses and extends our understanding of the mechanisms involved in root responses to abiotic tolerance in maize.
|
|
Received: 25 December 2019
Accepted:
|
| Fund: This work was supported by grants from the National Key Technology Research and Development Program of Ministry of Science and Technology of China (2016YFD0100303), the National Natural Science Foundation of China (31972487, 31902101 and 31801028), the Key Technology Research and Development Program of Jiangsu, China (BE2018325), the Natural Science Foundation of Jiangsu Province, China (BK20180920), and the project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD). |
|
Corresponding Authors:
Correspondence YANG Ze-feng, E-mail: zfyang@yzu.edu.cn; XU Chen-wu, E-mail: qtls@yzu.edu.cn
|
| About author:
* These authors contributed equally to this study. |
Cite this article:
LI Peng-cheng, YANG Xiao-yi, WANG Hou-miao, PAN Ting, YANG Ji-yuan, WANG Yun-yun, XU Yang, YANG Ze-feng, XU Chen-wu.
2021.
Metabolic responses to combined water deficit and salt stress in maize primary roots. Journal of Integrative Agriculture, 20(1): 109-119.
|
Abdelraheem A, Esmaeili N, Oconnell M A, Zhang J F. 2019. Progress and perspective on drought and salt stress tolerance in cotton. Industrial Crops and Products, 130, 118–129.
Bishopp A, Lynch J P. 2015. The hidden half of crop yields. Nature Plants, 1, 15117.
Chen T H H, Murata N. 2002. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Current Opinion in Plant Biology, 5, 250–257.
Cramer G R, Ergul A, Grimplet J, Tillett R L, Tattersall E A R, Bohlman M C, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D R, Schlauch K, Schooley D A, Cushman J C. 2007. Water and salinity stress in grapevines: Early and late changes in transcript and metabolite profiles. Functional & Integrative Genomics, 7, 111–134.
Das A, Rushton P J, Rohila J S. 2017. Metabolomic profiling of soybeans (Glycine max L.) reveals the importance of sugar and nitrogen metabolism under drought and heat stress. Plants (Basel), 6, 21.
Delauney A J, Verma D P S. 1993. Proline biosynthesis and osmoregulation in plants. The Plant Journal, 4, 215–223.
Fiehn O. 2002. Metabolomics - The link between genotypes and phenotypes. Plant Molecular Biology, 48, 155–171.
Hare P D, Cress W A, Van Staden J. 1998. Dissecting the roles of osmolyte accumulation during stress. Plant Cell and Environment, 21, 535–553.
Hayat S, Hayat Q, Alyemeni M N, Wani A S, Pichtel J, Ahmad A. 2012. Role of proline under changing environments: A review. Plant Signaling & Behavior, 7, 1456–1466.
Huang G T, Ma S L, Bai L P, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo Z F. 2012. Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports, 39, 969–987.
Jia W Q, Zhang L J, Wu D, Liu S, Gong X, Cui Z H, Cui N, Cao H Y, Rao L B, Wang C. 2015. Sucrose transporter AtSUC9 mediated by a low sucrose level is involved in Arabidopsis abiotic stress resistance by regulating sucrose distribution and ABA accumulation. Plant and Cell Physiology, 56, 1574–1587.
Jorge T F, Rodrigues J A, Caldana C, Schmidt R, Van Dongen J T, Thomas-Oates J, Antonio C. 2016. Mass spectrometry-based plant metabolomics: Metabolite responses to abiotic stress. Mass Spectrometry Reviews, 35, 620–649.
Julkowska M M, Hoefsloot H C J, Mol S, Feron R, De Boer G, Haring M A, Testerink C. 2014. Capturing Arabidopsis root architecture dynamics with ROOT-FIT reveals diversity in responses to salinity. Plant Physiology, 166, 1387–1402.
Julkowska M M, Koevoets I T, Mol S, Hoefsloot H C J, Feron R, Tester M, Keurentjes J J B, Korte A, Haring M A, De Boer G, Testerink C. 2017. Genetic components of root architecture remodeling in response to salt stress. The Plant Cell, 29, 3198–3213.
Kang Z, Babar M A, Khan N, Guo J, Khan J, Islam S, Shahi D. 2019. Comparative metabolomic profiling in the roots and leaves in contrasting genotypes reveals complex mechanisms involved in post-anthesis drought tolerance in wheat. PLoS ONE, 14, e0213502.
Koevoets I T, Venema J H, Elzenga J T M, Testerink C. 2016. Roots withstanding their environment: Exploiting root system architecture responses to abiotic stress to improve crop tolerance. Frontiers in Plant Science, 7, 1335.
Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie A R. 2006. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols, 1, 387–396.
Maeda H, Dudareva N. 2012. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annual Review of Plant Biology, 63, 73–105.
Motte H, Beeckman T. 2019. The evolution of root branching: Increasing the level of plasticity. Journal of Experimental Botany, 70, 785–793.
Muller B, Stosser M, Tardieu F. 1998. Spatial distributions of tissue expansion and cell division rates are related to irradiance and to sugar content in the growing zone of maize roots. Plant Cell and Environment, 21, 149–158.
Munns R. 2002. Comparative physiology of salt and water stress. Plant Cell and Environment, 25, 239–250.
Nam M H, Bang E, Kwon T Y, Kim Y, Kim E, Cho K, Park W J, Kim B, Yoon I S. 2015. Metabolite profiling of diverse rice germplasm and identification of conserved metabolic markers of rice roots in response to long-term mild salinity stress. International Journal of Molecular Sciences, 16, 21959–21974.
Opitz N, Marcon C, Paschold A, Malik W A, Lithio A, Brandt R, Piepho H P, Nettleton D, Hochholdinger F. 2016. Extensive tissue-specific transcriptomic plasticity in maize primary roots upon water deficit. Journal of Experimental Botany, 67, 1095–1107.
Osthoff A, Rose P D D, Baldauf J A, Piepho H, Hochholdinger F. 2019. Transcriptomic reprogramming of barley seminal roots by combined water deficit and salt stress. BMC Genomics, 20, 325.
Peleg Z, Apse M P, Blumwald E. 2011. Engineering salinity and water-stress tolerance in crop plants: Getting closer to the field. Advances in Botanical Research, 57, 405–443.
Pierik R, Testerink C. 2014. The art of being flexible: How to escape from shade, salt, and drought. Plant Physiology, 166, 5–22.
Rabara R C, Tripathi P, Rushton P J. 2017. Comparative metabolome profile between tobacco and soybean grown under water-stressed conditions. BioMed Research International, 2017, 3065251.
Ramesh S A, Tyerman S D, Xu B, Bose J, Kaur S, Conn V, Domingos P, Ullah S, Wege S, Shabala S, Feijo J A, Ryan P R, Gilliham M. 2015. GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nature Communications, 6, 7879.
Renault H, El Amrani A, Palanivelu R, Updegraff E P, Yu A, Renou J, Preuss D, Bouchereau A, Deleu C. 2011. GABA accumulation causes cell elongation defects and a decrease in expression of genes encoding secreted and cell wall-related proteins in Arabidopsis thaliana. Plant and Cell Physiology, 52, 894–908.
Rizhsky L, Liang H J, Shuman J L, Shulaev V, Davletova S, Mittler R. 2004. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology, 134, 1683–1696.
Ruan C J, Silva J A T. 2011. Metabolomics: Creating new potentials for unraveling the mechanisms in response to salt and drought stress and for the biotechnological improvement of xero-halophytes. Critical Reviews in Biotechnology, 31, 153–169.
Saini S, Sharma I, Kaur N, Pati P K. 2013. Auxin: A master regulator in plant root development. Plant Cell Reports, 32, 741–757.
Sami F, Yusuf M, Faizan M, Faraz A, Hayat S. 2016. Role of sugars under abiotic stress. Plant Physiology and Biochemistry, 109, 54–61.
Shelden M C, Dias D A, Jayasinghe N S, Bacic A, Roessner U. 2016. Root spatial metabolite profiling of two genotypes of barley (Hordeum vulgare L.) reveals differences in response to short-term salt stress. Journal of Experimental Botany, 67, 3731–3745.
Sun C X, Gao X X, Fu J Q, Zhou J H, Wu X F. 2015. Metabolic response of maize (Zea mays L.) plants to combined drought and salt stress. Plant and Soil, 388, 99–117.
Suzuki N, Rivero R M, Shulaev V, Blumwald E, Mittler R. 2014. Abiotic and biotic stress combinations. New Phytologist, 203, 32–43.
Sweetlove L J, Beard K F M, Nunesnesi A, Fernie A R, Ratcliffe R G. 2010. Not just a circle: Flux modes in the plant TCA cycle. Trends in Plant Science, 15, 462–470.
Ullah N, Yuce M, Gokce Z N O, Budak H. 2017. Comparative metabolite profiling of drought stress in roots and leaves of seven Triticeae species. BMC Genomics, 18, 969.
Upchurch R G. 2008. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters, 30, 967–977.
Wang P, Wang Z K, Pan Q C, Sun X C, Chen H, Chen F J, Yuan L X. 2019. Increased biomass accumulation in maize grown in mixed nitrogen supply is mediated by auxin synthesis. Journal of Experimental Botany, 70, 1859–1873.
Widodo, Patterson J H, Newbigin E, Tester M, Bacic A, Roessner U. 2009. Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. Journal of Experimental Botany, 60, 4089–4103.
Wu D Z, Cai S G, Chen M X, Ye L Z, Chen Z G, Zhang H T, Dai F, Wu F B, Zhang G P. 2013. Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS ONE, 8, e55431.
Xie T T, Ji J, Chen W, Yue J Y, Du C J, Sun J C, Chen L Z, Jiang Z P, Shi S Q. 2020. GABA negatively regulates adventitious root development. Journal of Experimental Botany, 71, 1459–1474.
Zazimalova E, Napier R M. 2003. Points of regulation for auxin action. Plant Cell Reports, 21, 625–634.
Zhang M, Liang X, Wang L, Cao Y, Song W, Shi J, Lai J, Jiang C. 2019. A HAK family Na+ transporter confers natural variation of salt tolerance in maize. Nature Plants, 5, 1297–1308.
Zhang M L, Kong X P, Xu X B, Li C L, Tian H Y, Ding Z J. 2015. Comparative transcriptome profiling of the maize primary, crown and seminal root in response to salinity stress. PLoS ONE, 10, e0121222.
Zhao X, Wang W, Zhang F, Deng J, Li Z, Fu B. 2014. Comparative metabolite profiling of two rice genotypes with contrasting salt stress tolerance at the seedling stage. PLoS ONE, 9, e108020.
|
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
