Genome-scale characterization of the vacuole nitrate transporter Chloride Channel (CLC) genes and their transcriptional responses to diverse nutrient stresses in allotetraploid rapeseed

Liao, Qiong; Zhou, Ting; Yao, Junyue; Han, Qing-Fen; Song, Haixing; Guan, Chunyun; Hua, Yingpeng; Zhang, Zhenhua

doi:10.1371/journal.pone.0208648

Cited by 24 publications

(19 citation statements)

References 80 publications

(135 reference statements)

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“…Based on the sequence homology, 10 genes encoding CLCs have been identified in Oryza sativa (Kushwaha et al ., 2009), 17 in Nicotiana tabacum (Zhang et al ., 2018), 8 in Camellia sinensis (Xing et al ., 2020), 11 CLCs in Brassica rapa , 10 in B. oleracea , and 22 in B. napus (Liao et al ., 2018), 7 in Suaeda fruticosa (Nedelyaeva et al ., 2018) and 8 in Glycine max (Wei et al ., 2019). Just as AtCLCs, most of these proteins form a major phylogenetic group (subclass I), while a few CLCs like AtCLC‐e and AtCLC‐f form a separate group (subclass II) and are closely related to bacterial CLCs.…”

Section: Clcs In Plantsmentioning

confidence: 99%

“…As in Arabidopsis, Brassica napus BnaCLC‐a members ( BnaCLC‐a1‐4 ; sharing sequence similarity with AtCLC‐a ) showed strong induction of gene expression in both shoots and roots after NO 3 − replenishment following N starvation. BnaCLC‐b was induced in the shoots by NO 3 , while BnaCLC‐c to ‐ g members were either down‐regulated or showed no changes to NO 3 − treatment (Liao et al ., 2018). Even in Suaeda altissima , a euhalophyte plant, the expression of SaCLC‐a1 (that shares sequence similarity with AtCLC‐a and AtCLC‐b ) increased in the roots in response to nitrate‐deficiency (Nedelyaeva et al ., 2019).…”

Section: Clcs In Plantsmentioning

confidence: 99%

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The chloride channels: Silently serving the plants

Subba

Tomar

Pareek

et al. 2020

Physiologia Plantarum

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Chloride channels (CLCs), member of anion transporting proteins, are present ubiquitously in all life forms. Diverging from its name, the CLC family includes both channel and exchanger (proton‐coupled) proteins; nevertheless, they share conserved structural organization. They are engaged in diverse indispensable functions such as acid and fluoride tolerance in prokaryotes to muscle stabilization, transepithelial transport, and neuronal development in mammals. Mutations in genes encoding CLCs lead to several physiological disorders in different organisms, including severe diseases in humans. Even in plants, loss of CLC protein function severely impairs various cellular processes critical for normal growth and development. These proteins sequester Cl− into the vacuole, thus, making them an attractive target for improving salinity tolerance in plants caused by high abundance of salts, primarily NaCl. Besides, some CLCs are involved in NO3− transport and storage function in plants, thus, influencing their nitrogen use efficiency. However, despite their high significance, not many studies have been carried out in plants. Here, we have attempted to concisely highlight the basic structure of CLC proteins and critical residues essential for their function and classification. We also present the diverse functions of CLCs in plants from their first cloning back in 1996 to the knowledge acquired as of now. We stress the need for carrying out more in‐depth studies on CLCs in plants, for they may have future applications towards crop improvement.

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Section: Clcs In Plantsmentioning

confidence: 99%

Section: Clcs In Plantsmentioning

confidence: 99%

The chloride channels: Silently serving the plants

Subba

Tomar

Pareek

et al. 2020

Physiologia Plantarum

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“…The Arabidopsis thaliana wild-type Columbia-0 (Col-0) was used as a control for the tonoplast V- relative humidity and a constant temperature of 22 °C. Seeds were sown in a matrix consisting of vermiculite and perlite at a ratio of 3:2, and allowed to germinate and grow for 10 d [36,37].…”

Section: Methodsmentioning

confidence: 99%

Growth Retardation Caused by Reduced Tonoplast V-ATPase Activity in Arabidopsis thaliana

Liang¹,

Liu²,

Xiao³

et al. 2020

Preprint

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Background: Vacuoles are unique compartments in plant cells. Their multiple functions require massive fluxes of molecules across their limiting membrane, the tonoplast. Transport across the tonoplast is energized by its membrane potential and the proton gradient established by two proton pumps, the vacuolar H+-ATPase (V-ATPase), and the vacuolar H+-pyrophosphatase (V-PPase), which play important roles in the growth and development of plants. However, the mechanisms by which they affect plant growth and development, in the absence of tonoplast proton pumps, remain unclear. Results: In this study, we show that the Arabidopsis thaliana double mutant, vha-a2vha-a3, which lacks two tonoplast-localized isoforms of the membrane-integral V-ATPase subunit VHA-a, is viable, but shows a phenotype of inhibited growth and leaf chlorosis. Reduced total nitrogen absorption and increased nitrate assimilation lead to the accumulation of ammonium in the shoot, which results in the growth retardation of vha-a2vha-a3. Concurrently, the distribution and concentration of cations are abnormal in plants when VHA-a2 and VHA-a3 genes are absent, which is another major growth-limiting factor. Interestingly, the growth inhibition of the vha-a2vha-a3 double mutant was alleviated and senescence delayed, while the concentration of total nitrogen increased and that of ammonium decreased, when adding additional potassium. Conclusions: Our results show that plants can be viable without VHA-a2 and VHA-a3 but are affected by multiple factors that result in growth retardation, which can be alleviated by adding additional potassium, which provides a new insight on the relationship between vacuolar H+-ATPase and potassium.

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“…Concentrations of mineral elements were quantified by ICP-MS (NexION TM 350X; PerkinElmer, Massachusetts, USA). Fresh tissues of rapeseed plants were sampled and bathed in boiling water for 30 min; then, they were assayed for nitrate concentrations using a continuous flow autoanalyzer (AA3, Seal Analytical Inc., Southampton, UK) [ 76 ]. After treatment at 120 °C for 30 min, the samples were dried at 65 °C for 72 h, and then were milled to a fine powder.…”

Section: 2 Quantification Of Morpho-physiological Characteristicsmentioning

confidence: 99%

Genome-Wide Differential DNA Methylation and miRNA Expression Profiling Reveals Epigenetic Regulatory Mechanisms Underlying Nitrogen-Limitation-Triggered Adaptation and Use Efficiency Enhancement in Allotetraploid Rapeseed

Hua

Zhou

Huang

et al. 2020

IJMS

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Improving crop nitrogen (N) limitation adaptation (NLA) is a core approach to enhance N use efficiency (NUE) and reduce N fertilizer application. Rapeseed has a high demand for N nutrients for optimal plant growth and seed production, but it exhibits low NUE. Epigenetic modification, such as DNA methylation and modification from small RNAs, is key to plant adaptive responses to various stresses. However, epigenetic regulatory mechanisms underlying NLA and NUE remain elusive in allotetraploid B. napus. In this study, we identified overaccumulated carbohydrate, and improved primary and lateral roots in rapeseed plants under N limitation, which resulted in decreased plant nitrate concentrations, enhanced root-to-shoot N translocation, and increased NUE. Transcriptomics and RT-qPCR assays revealed that N limitation induced the expression of NRT1.1, NRT1.5, NRT1.7, NRT2.1/NAR2.1, and Gln1;1, and repressed the transcriptional levels of CLCa, NRT1.8, and NIA1. High-resolution whole genome bisulfite sequencing characterized 5094 differentially methylated genes involving ubiquitin-mediated proteolysis, N recycling, and phytohormone metabolism under N limitation. Hypermethylation/hypomethylation in promoter regions or gene bodies of some key N-metabolism genes might be involved in their transcriptional regulation by N limitation. Genome-wide miRNA sequencing identified 224 N limitation-responsive differentially expressed miRNAs regulating leaf development, amino acid metabolism, and plant hormone signal transduction. Furthermore, degradome sequencing and RT-qPCR assays revealed the miR827-NLA pathway regulating limited N-induced leaf senescence as well as the miR171-SCL6 and miR160-ARF17 pathways regulating root growth under N deficiency. Our study provides a comprehensive insight into the epigenetic regulatory mechanisms underlying rapeseed NLA, and it will be helpful for genetic engineering of NUE in crop species through epigenetic modification of some N metabolism-associated genes.

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Genome-scale characterization of the vacuole nitrate transporter Chloride Channel (CLC) genes and their transcriptional responses to diverse nutrient stresses in allotetraploid rapeseed

Cited by 24 publications

References 80 publications

The chloride channels: Silently serving the plants

The chloride channels: Silently serving the plants

Growth Retardation Caused by Reduced Tonoplast V-ATPase Activity in Arabidopsis thaliana

Genome-Wide Differential DNA Methylation and miRNA Expression Profiling Reveals Epigenetic Regulatory Mechanisms Underlying Nitrogen-Limitation-Triggered Adaptation and Use Efficiency Enhancement in Allotetraploid Rapeseed

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