Zhong Shan, Yanli Chu, Guangfang Sun, Rui Chen, Jun Yan, Qiwei He, Yingna Liu, Bin Wang, Mingda Luan, Wenzhi Lan
{"title":"Mechanisms of vacuolar phosphate efflux supporting soybean root hair growth in response to phosphate deficiency","authors":"Zhong Shan, Yanli Chu, Guangfang Sun, Rui Chen, Jun Yan, Qiwei He, Yingna Liu, Bin Wang, Mingda Luan, Wenzhi Lan","doi":"10.1111/jipb.13735","DOIUrl":null,"url":null,"abstract":"<div>\n \n <p>Phosphorus is an essential macronutrient for plant growth and development. In response to phosphate (Pi) deficiency, plants rapidly produce a substitutive amount of root hairs; however, the mechanisms underlying Pi supply for root hair growth remain unclear. Here, we observed that soybean (<i>Glycine max</i>) plants maintain a consistent level of Pi within root hairs even under external Pi deficiency. We therefore investigated the role of vacuole-stored Pi, a major Pi reservoir in plant cells, in supporting root hair growth under Pi-deficient conditions. Our findings indicated that two vacuolar Pi efflux (VPE) transporters, GmVPE1 and GmVPE2, remobilize vacuolar stored Pi to sustain cytosolic Pi content in root hair cells. Genetic analysis showed that double mutants of <i>GmVPE1</i> and <i>GmVPE2</i> exhibited reduced root hair growth under low Pi conditions. Moreover, <i>GmVPE1</i> and <i>GmVPE2</i> were highly expressed in root hairs, with their expression levels significantly upregulated by low Pi treatment. Further analysis revealed that GmRSL2 (ROOT HAIR DEFECTIVE 6-like 2), a transcription factor involved in root hair morphogenesis, directly binds to the promoter regions of <i>GmVPE1</i> and <i>GmVPE2</i>, and promotes their expressions under low Pi conditions. Additionally, mutants lacking both <i>GmRSL2</i> and its homolog <i>GmRSL3</i> exhibited impaired root hair growth under low Pi stress, which was rescued by overexpressing either <i>GmVPE1</i> or <i>GmVPE2</i>. Taken together, our study has identified a module comprising vacuolar Pi exporters and transcription factors responsible for remobilizing vacuolar Pi to support root hair growth in response to Pi deficiency in soybean.</p></div>","PeriodicalId":195,"journal":{"name":"Journal of Integrative Plant Biology","volume":null,"pages":null},"PeriodicalIF":9.3000,"publicationDate":"2024-07-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/jipb.13735","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Integrative Plant Biology","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/jipb.13735","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Phosphorus is an essential macronutrient for plant growth and development. In response to phosphate (Pi) deficiency, plants rapidly produce a substitutive amount of root hairs; however, the mechanisms underlying Pi supply for root hair growth remain unclear. Here, we observed that soybean (Glycine max) plants maintain a consistent level of Pi within root hairs even under external Pi deficiency. We therefore investigated the role of vacuole-stored Pi, a major Pi reservoir in plant cells, in supporting root hair growth under Pi-deficient conditions. Our findings indicated that two vacuolar Pi efflux (VPE) transporters, GmVPE1 and GmVPE2, remobilize vacuolar stored Pi to sustain cytosolic Pi content in root hair cells. Genetic analysis showed that double mutants of GmVPE1 and GmVPE2 exhibited reduced root hair growth under low Pi conditions. Moreover, GmVPE1 and GmVPE2 were highly expressed in root hairs, with their expression levels significantly upregulated by low Pi treatment. Further analysis revealed that GmRSL2 (ROOT HAIR DEFECTIVE 6-like 2), a transcription factor involved in root hair morphogenesis, directly binds to the promoter regions of GmVPE1 and GmVPE2, and promotes their expressions under low Pi conditions. Additionally, mutants lacking both GmRSL2 and its homolog GmRSL3 exhibited impaired root hair growth under low Pi stress, which was rescued by overexpressing either GmVPE1 or GmVPE2. Taken together, our study has identified a module comprising vacuolar Pi exporters and transcription factors responsible for remobilizing vacuolar Pi to support root hair growth in response to Pi deficiency in soybean.
磷是植物生长和发育所必需的重要营养元素。为应对磷酸盐(Pi)缺乏,植物会迅速产生替代量的根毛;然而,根毛生长的 Pi 供应机制仍不清楚。在这里,我们观察到大豆(Glycine max)植株即使在外部 Pi 缺乏的情况下也能在根毛中保持稳定的 Pi 水平。因此,我们研究了液泡储存的 Pi(植物细胞中主要的 Pi 储存库)在 Pi 缺乏条件下支持根毛生长的作用。我们的研究结果表明,两个液泡态 Pi 外排(VPE)转运体(GmVPE1 和 GmVPE2)可重新动员液泡储存的 Pi,以维持根毛细胞中的细胞质 Pi 含量。遗传分析表明,在低 Pi 条件下,GmVPE1 和 GmVPE2 的双突变体表现出根毛生长减弱。此外,GmVPE1 和 GmVPE2 在根毛中高度表达,其表达水平在低 Pi 处理下显著上调。进一步分析发现,参与根毛形态发生的转录因子 GmRSL2(ROOT HAIR DEFECTIVE 6-like 2)直接与 GmVPE1 和 GmVPE2 的启动子区域结合,并在低 Pi 条件下促进它们的表达。此外,缺乏 GmRSL2 及其同源基因 GmRSL3 的突变体在低 Pi 胁迫下表现出根毛生长受损,而过表达 GmVPE1 或 GmVPE2 则可挽救这种受损。综上所述,我们的研究发现了一个由液泡态 Pi 导出器和转录因子组成的模块,该模块负责重新动员液泡态 Pi 以支持大豆根毛在 Pi 缺乏时的生长。
期刊介绍:
Journal of Integrative Plant Biology is a leading academic journal reporting on the latest discoveries in plant biology.Enjoy the latest news and developments in the field, understand new and improved methods and research tools, and explore basic biological questions through reproducible experimental design, using genetic, biochemical, cell and molecular biological methods, and statistical analyses.