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ABA homeostasis and long-distance translocation are redundantly regulated by ABCG ABA importers.

ABSTRACT: The effects of abscisic acid (ABA) on plant growth, development, and response to the environment depend on local ABA concentrations. Here, we show that in Arabidopsis, ABA homeostasis is regulated by two previously unknown ABA transporters. Adenosine triphosphate–binding cassette subfamily G member 17 (ABCG17) and ABCG18 are localized to the plasma membranes of leaf mesophyll and cortex cells to redundantly promote ABA import, leading to conjugated inactive ABA sinks, thus restricting stomatal closure. ABCG17 and ABCG18 double knockdown revealed that the transporters encoded by these genes not only limit stomatal aperture size, conductance, and transpiration while increasing water use efficiency but also control ABA translocation from the shoot to the root to regulate lateral root emergence. Under abiotic stress conditions, ABCG17 and ABCG18 are transcriptionally repressed, promoting active ABA movement and response. The transport mechanism mediated by ABCG17 and ABCG18 allows plants to maintain ABA homeostasis under normal growth conditions.

SUBMITTER: Zhang Y

PROVIDER: S-EPMC8528425 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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ABA homeostasis and long-distance translocation are redundantly regulated by ABCG ABA importers.

Zhang Yuqin Y Kilambi Himabindu Vasuki HV Liu Jie J Bar Hamutal H Lazary Shani S Egbaria Aiman A Ripper Dagmar D Charrier Laurence L Belew Zeinu Mussa ZM Wulff Nikolai N Damodaran Suresh S Nour-Eldin Hussam Hassan HH Aharoni Asaph A Ragni Laura L Strader Lucia L Sade Nir N Weinstain Roy R Geisler Markus M Shani Eilon E

Science advances 20211020 43

The effects of abscisic acid (ABA) on plant growth, development, and response to the environment depend on local ABA concentrations. Here, we show that in <i>Arabidopsis</i>, ABA homeostasis is regulated by two previously unknown ABA transporters. Adenosine triphosphate–binding cassette subfamily G member 17 (ABCG17) and ABCG18 are localized to the plasma membranes of leaf mesophyll and cortex cells to redundantly promote ABA import, leading to conjugated inactive ABA sinks, thus restricting sto ...[more]

PMID: 34669479

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Project description:The plant hormone abscisic acid (ABA) is able to regulate the expression of ABA-responsive genes via signaling transduction, and thus plays an important role in regulating plant responses to abiotic stresses. Hence, characterization of unknown ABA response genes may enable us to identify novel regulators of ABA and abiotic stress responses. By using RT-PCR analysis, we found that the expression levels of ABA-induced Serine-rich Repressor 1 (ASR1)and ASR2, two closely related unknown function genes, were increased in response to ABA treatment. Amino acid sequence analyses show that ASR1 contains an L×L×L motif and both ASR1 and ASR2 are enriched in serine. Transfection assays in Arabidopsis leaf protoplasts show that ASR1 and ASR2 were predominantly localized in the nucleus and were able to repress the expression of the reporter gene. The roles of ASRs in regulating ABA responses were examined by generating transgenic Arabidopsis plants over-expressing ASR1 and ASR2, respectively, and CRISPR/Cas9 gene-edited single and double mutants for ASR1 and ASR2. In both the seed germination and cotyledon greening assays, ABA sensitivity remained largely unchanged in the over-expression transgenic plants and the single mutants of ASR1 and ASR2, but greatly increased ABA sensitivity was observed in the asr1 asr2 double mutants. In root elongation assays, however, decreased ABA sensitivity was observed in the 35S:ASR1 and 35S:ASR2 transgenic plants, whereas increased ABA sensitivity was observed in the asr1 and asr2 single mutants, and ABA sensitivity was further increased in the asr1 asr2 double mutants. Transcriptome analysis show that the differentially expressed genes (DEGs) down-regulated in the 35S:ASR1 transgenic plant seedlings, but up-regulated in the asr1 asr2 double mutant seedlings were highly enriched in processes including responses to plant hormones and stress stimuli. Taken together, our results show that ASR1 and ASR2 are closely related ABA response genes, ASR1 and ASR2 are serine-rich novel transcription repressors, and they negatively regulate ABA responses in Arabidopsis in a redundant manner.

Project description:ABA is an important messenger that acts as a signaling mediator for regulating the adaptive response of plants to drought stress. Two production pathways, de novo biosynthesis and hydrolysis of glucose-conjugated ABA by β-glucosidase (BG), increase cellular ABA levels in plants. ABA catabolism via hydroxylation by 8'-hydroxylase (CYP707A), or conjugation by uridine diphosphate glucosyltransferase (UGT), decreases cellular ABA levels. The transport of ABA through ATP-binding cassette (ABC)-containing transporter proteins, members of ABC transporter G family (ABCG), across plasma membrane (PM) is another important pathway to regulate cellular ABA levels. In this study, based on our previously constructed transcriptome of peanut leaves in response to drought stress, fourteen candidate genes involved in ABA production (including AhZEP, AhNCED1 and AhNCED3, AhABA2, AhAAO1 and AhAAO2, AhABA3, AhBG11 and AhBG24), catabolism (including AhCYP707A3, AhUGT71K1 and AhUGT73B4) and transport (including AhABCG22-1 and AhABCG22-2), were identified homologously and phylogenetically, and further analyzed at the transcriptional level by real-time RT-PCR, simultaneously determining ABA levels in peanut leaves in response to drought. The high sequence identity and very similar subcellular localization of the proteins deduced from 14 identified genes involved in ABA production, catabolism and transport with the reported corresponding enzymes in databases suggest their similar roles in regulating cellular ABA levels. The expression analysis showed that the transcripts of AhZEP, AhNCED1, AhAAO2 and AhABA3 instead of AhABA2, AhNCED3 and AhAAO1 in peanut leaves increased significantly in response to drought stress; and that the AhBG11 and AhBG24 mRNA levels were rapidly and significantly up-regulated, with a 4.83- and 4.58-fold increase, respectively at 2-h of drought stress. The genes involved in ABA catabolism AhCYP707A3, AhUGT71K1 instead of AhUGT73B4 were significantly induced in response to drought stress. The expression of two closely related peanut ABCG genes, AhABCG22.1 and AhABCG22.2, was significantly up-regulated in response to drought stress. The ABA levels rapidly began to accumulate within 2 h (a 56.6-fold increase) from the start of drought stress, and peaked at 10 h of the stress. The highly and rapidly stress up-regulated expressions of genes involved in ABA production and transport, particularly AhNCED1, AhBG11 and AhBG24, and AhABCG22.1 and AhABCG22.2, might contribute to the rapid ABA accumulation in peanut leaves in response to drought. In response to drought stress, ABA accumulation levels in peanut leaves agree well with the up-regulated expressions of ABA-producing genes (AhZEP, AhNCED1, AhAAO2, AhABA3, AhBG11 and AhBG24) and PM-localized ABA importer genes (AhABCG22-1 and AhABCG22-2), in spite of the simultaneously induced ABA catabolic genes (AhCYP707A3 and AhUGT71K1), although the induction of catabolic genes was much lower than that of biosynthetic gene (AhNCED1). This difference in induction kinetics of gene expression may define the significant accumulation of drought-induced ABA levels. These results suggest that ABA homeostasis in peanut leaves in response to drought maintained through a balance between the production, catabolism and transport, rather than simply by the biosynthesis.

Project description:The Gram-positive model bacterium B. subtilis is able to import all proteinogenic amino acids from the environment as well as to synthesize them. However, the players involved in the acquisition of asparagine have not yet been identified for this bacterium. In this work, we used d-asparagine as a toxic analog of l-asparagine to identify asparagine transporters. This revealed that d- but not l-asparagine is taken up by the malate/lactate antiporter MleN. Specific strains that are sensitive to the presence of l-asparagine due to the lack of the second messenger cyclic di-AMP or due to the intracellular accumulation of this amino acid were used to isolate and characterize suppressor mutants that were resistant to the presence of otherwise growth-inhibiting concentrations of l-asparagine. These screens identified the broad-spectrum amino acid importers AimA and BcaP as responsible for the acquisition of l-asparagine. The amino acid exporter AzlCD allows detoxification of l-asparagine in addition to 4-azaleucine and histidine. This work supports the idea that amino acids are often transported by promiscuous importers and exporters. However, our work also shows that even stereo-enantiomeric amino acids do not necessarily use the same transport systems.IMPORTANCETransport of amino acid is a poorly studied function in many bacteria, including the model organism Bacillus subtilis. The identification of transporters is hampered by the redundancy of transport systems for most amino acids as well as by the poor specificity of the transporters. Here, we apply several strategies to use the growth-inhibitive effect of many amino acids under defined conditions to isolate suppressor mutants that exhibit either reduced uptake or enhanced export of asparagine, resulting in the identification of uptake and export systems for l-asparagine. The approaches used here may be useful for the identification of transporters for other amino acids both in B. subtilis and in other bacteria.

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ABA homeostasis and long-distance translocation are redundantly regulated by ABCG ABA importers.

Publications

ABA homeostasis and long-distance translocation are redundantly regulated by ABCG ABA importers.

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