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Journal of Integrative Agriculture
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Comparative transcriptome and lipidome reveal that low K+ signal effectively alleviate the effect induced by Ca2+ deficiency in fiber of cotton (Gossypium hirsutum)
GUO Kai1*, GAO Wei2*, ZHANG Tao-rui1, WANG Zu-ying1, SUN Xiao-ting1, YANG Peng1, LONG Lu2, LIU Xue-ying1, WANG Wen-wen1, TENG Zhong-hua1, LIU Da-jun1, LIU De-xin1, TU Li-li3, ZHANG Zheng-sheng1

1 College of Agronomy and Biotechnology, Southwest University, Chongqing 400716, P.R.China

2 State Key Laboratory of Cotton Biology, Henan Key Laboratory of Plant Stress Biology, School of Life Sciences, Henan University, Kaifeng, P.R.China

3 National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, P.R.China

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摘要  

Ca2+离子在维持细胞壁以及细胞膜的完整性中具有重要作用,是植物生长和发育中必不可少的矿质营养元素之一。解析Ca2+离子在糖代谢和脂代谢中的作用能够为理解棉花纤维快速伸长阶段细胞膜和细胞壁的动态变化提供有意义的参考。本研究利用胚珠培养系统发现缺Ca2+会促进纤维和胚珠细胞的膨大,但同时也会诱导组织的褐化。RNA-seq差异表达基因分析发现缺Ca2+使细胞处于一个较高的氧化态,并且激活与糖代谢和脂代谢相关的基因的表达。尤其以糖酵解途径变化最为显著,其代谢途径中的9个酶相关的基因上调表达,缺Ca2+处理细胞中的葡萄糖含量显著下降,改变了糖酵解途径的流动。低K+能够恢复缺Ca2+诱导糖酵解途径相关基因的表达以及葡萄糖的含量。采用电喷雾电离串联质谱技术检测了不同Ca2+K+离子处理条件下细胞中脂质组成分的动态变化。缺Ca2+处理细胞中自由脂肪酸(FA)、二酰甘油(DAG)和糖脂含量降低,三酰甘油(DAG)磷脂酰乙醇胺(PE)、磷脂酰甘油(PG)、磷脂酰胆碱(PC含量增加。低K+与缺Ca2+的互作信号能够恢复FA、磷脂、糖脂含量至正常水平,有效缓解缺Ca2+效应。本研究通过在转录和代谢水平的比较分析,揭示了Ca2+K+信号互作在维持纤维快速伸长过程中糖酵解和脂代谢中发挥着重要作用。



Abstract  

Calcium (Ca2+) plays important roles in determining plant growth and development owing to its function in maintaining cell wall and membrane integrity.  Therefore, understanding the role of Ca2+ in carbon and lipid metabolism could provide insights into the dynamic changes of cell membranes and cell walls during rapid elongation of cotton fibers.  In the present study, we found that the lack of Ca2+ promoted fiber elongation and ovule rapid expansion, but also caused tissue browning in ovule culture system.  RNA-sequencing revealed that Ca2+ deficiency induced cells to be in a highly oxidized state, and the expression of genes related to carbon metabolism and lipid metabolism was activated significantly.  All gene members of 9 key enzymes involving in glycolysis were up-regulated, and glucose was significantly reduced in Ca2+ deficiency treated tissues.  Ca2+ deficiency adjusted the flowing of glycolysis metabolic.  However, low K+ recovered the expression levels of glycolysis genes and glucose content caused by Ca2+ deficiency.  Electrospray ionization-tandem mass spectrometry technology was applied to uncover the dynamic profile of lipidome under Ca2+ and K+ interacted condition.  Ca2+ deficiency led to the decrease of fatty acid (FA), diacylglycerol (DAG) and glycolipid, and the significant increase of triacylglycerol (TAG), phospholipid PE (phosphatidylethanolamine), PG (phosphatidylglycerol) and PC (phosphatidylcholine).  Low K+ restored the contents of FA, phospholipids and glycolipids, effectively relieved the symptoms caused by Ca2+ deficiency, and recovered the development of fiber cells.  This study revealed dynamic changes in transcript and metabolic levels, and uncovered the signaling interaction of Ca2+ deficiency and low K+ in glycolysis and lipid metabolism during fiber development.

Keywords:  cotton fiber        glycolysis       lipidome        calcium        potassium  
Online: 10 January 2023  
Fund: 

This project was supported by the National Natural Science Foundation of China (31901577), the Fundamental Research Funds for the Central Universities (SWU-KT22035) and the State Key Laboratory of Cotton Biology Open Fund (CB2021A32).

About author:  Correspondence ZHANG Zheng-sheng, E-mail: zhangzs@swu.edu.cn * These authors have contributed equally to this work.

Cite this article: 

GUO Kai, GAO Wei, ZHANG Tao-rui, WANG Zu-ying, SUN Xiao-ting, YANG Peng, LONG Lu, LIU Xue-ying, WANG Wen-wen, TENG Zhong-hua, LIU Da-jun, LIU De-xin, TU Li-li, ZHANG Zheng-sheng. 2023. Comparative transcriptome and lipidome reveal that low K+ signal effectively alleviate the effect induced by Ca2+ deficiency in fiber of cotton (Gossypium hirsutum). Journal of Integrative Agriculture, Doi:10.1016/j.jia.2023.01.002

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