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Summary: Drought is a deleterious abiotic stress factor that constrains crop growth and development. Post‐translational modification of proteins mediated by the ubiquitin–proteasome system is an effective strategy for directing plant responses to stress, but the regulatory mechanisms in wheat remain unclear. In this study, we showed that TaSDIR1‐4A is a positive modulator of the drought response. Overexpression of TaSDIR1‐4A increased the hypersensitivity of stomata, root length and endogenous abscisic acid (ABA) content under drought conditions. TaSDIR1‐4A encodes a C3H2C3‐type RING finger protein with E3 ligase activity. Amino acid mutation in its conserved domain led to loss of activity and altered the subcellular localization. The membrane‐bound transcription factor TaWRKY29 was identified by yeast two‐hybrid screening, and it was confirmed as interacting with TaSDIR1‐4A both in vivo and in vitro. TaSDIR1‐4A mediated the polyubiquitination and proteolysis of the C‐terminal amino acid of TaWRKY29, and its translocation from the plasma membrane to the nucleus. Activated TaWRKY29 bound to the TaABI5 promoter to stimulate its expression, thereby positively regulating the ABA signalling pathway and drought response. Our findings demonstrate the positive role of TaSDIR1‐4A in drought tolerance and provide new insights into the involvement of UPS in the wheat stress response. [ABSTRACT FROM AUTHOR]

Genetic strategies can be effective in improving wheat (Triticum aestivum L.) drought stress tolerance, but accumulating evidence suggests that overexpressing drought-resistance genes, especially genes related to the abscisic acid (ABA) signaling pathway, can retard plant growth. We previously characterized the positive roles of the wheat bZIP transcription factor TaFD-Like2-1A (TaFDL2-1A) in drought stress tolerance and ABA biosynthesis and response, whereas a dwarfing shoot exhibited under normal conditions. This study determined the underlying mechanisms that allow TaFDL2-1A to affect shoot growth. Overexpressing TaFDL2-1A decreased cell length, cell width, leaf size, shoot length, and biomass in wheat. The results of RNA-seq showed that multiple differently expressed transcripts are enriched in the auxin signaling pathway. Further analysis indicated higher expression levels of Gretchen Hagen3 (GH3) genes and lower indole-3-acetic acid (IAA) concentrations in the TaFDL2-1A overexpression lines. Exogenous IAA treatment restored the phenotypes of the TaFDL2-1A overexpression lines to wild-type levels. Transcriptional regulation analysis suggested that TaFDL2-1A enhances the expression of auxin metabolism genes, such as TaGH3.2-3A, TaGH3.2-3B, TaGH3.8-2A, and TaGH3.8-2D, by directly binding to ACGT core cis-elements. Furthermore, tafdl2 knock-out plants had lower expression levels of these GH3 genes and higher IAA levels than Fielder wheat. These GH3 gene expression and IAA levels were induced and reduced in Fielder wheat and tafdl2 knock-out plants treated with exogenous ABA. Our findings elucidate mechanisms underlying the functional redundancy of TaFDL2-1A in the crosstalk between ABA and IAA to affect shoot growth and provide insights into the balance between drought resistance and yield in wheat., (© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.)