Triple-localized WHIRLY2 Influences Leaf Senescence and Silique Development via Carbon Allocation

Huang, Chenxing; Yu, Jinfa; Cai, Qi; Chen, Yuxiang; Li, Yanyun; Ren, Yujun; Miao, Ying

doi:10.1104/pp.20.00832

Cited by 31 publications

(45 citation statements)

References 66 publications

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“…The action of WHY1 as a transcription factor in the nucleus also regulates the expression of genes associated with photosynthesis and carbon metabolism. For example, WHY1 binds to the promoter of the rbcS gene that encodes the small subunit of the potato ribulose-1, 5-carboxylase, oxygenase under cold stress [ 80 ], while WHY2 binds to the promoters of the SWEET11/15 genes that encode sucrose transporters, leading to the modulation of starch allocation and silique development [ 17 ]. Here we report that the absence of WHY1 has a significant impact on the levels of transcripts encoding enzymes associated with the Calvin cycle, starch and sugar metabolism, glycolysis, the TCA cycle and amino acid metabolism, many of which were more abundant in WHY1-deficient leaves than the wild type.…”

Section: Discussionmentioning

confidence: 99%

“…However, the intracellular localisation of the WHY proteins appears to be flexible and determined by developmental and environmental signals. For example, the WHY2 protein that is primarily associated with mitochondrial nucleoids, was found in mitochondria, chloroplasts and nuclei during leaf senescence [ 17 ]. Moreover, it appears that WHY3 can compensate for WHY2 in the Arabidopsis why 2-1 mutant because WHY3 can be targeted to both chloroplasts and mitochondria [ 18 ].…”

Section: Introductionmentioning

confidence: 99%

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WHIRLY1 functions in the nucleus to regulate barley leaf development and associated metabolite profiles

Karpińska

Razak

James

et al. 2022

Biochemical Journal

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The WHIRLY (WHY) DNA/RNA binding proteins fulfil multiple but poorly characterised functions in leaf development. Here we show that WHY1 transcript levels were highest in the bases of 7-day old barley leaves. Immunogold labelling revealed that the WHY1 protein was more abundant in the nuclei than the proplastids of the leaf bases. To identify transcripts associated with leaf development we conducted hierarchical clustering of differentially abundant transcripts along the developmental gradient of wild-type leaves. Similarly, metabolite profiling was employed to identify metabolites exhibiting a developmental gradient. A comparative analysis of transcripts and metabolites in barley lines (W1-1 and W1-7) lacking WHY1, which show delayed greening compared to the wild type revealed that the transcript profile of leaf development was largely unchanged in W1-1 and W1-7 leaves. However, there were differences in levels of several transcripts encoding transcription factors associated with chloroplast development. These include a barley homologue of the Arabidopsis GATA transcription factor that regulates stomatal development, greening and chloroplast development, NAC1; two transcripts with similarity to Arabidopsis GLK1 and two transcripts encoding ARF transcriptions factors with functions in leaf morphogenesis and development. Chloroplast proteins were less abundant in the W1-1 and W1-7 leaves than the wildtype. The levels of tricarboxylic acid cycle metabolites and GABA were significantly lower in WHY1 knockdown leaves than the wild type. This study provides evidence that WHY1 is localized in the nuclei of leaf bases, contributing the regulation of nuclear-encoded transcripts that regulate chloroplast development.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

WHIRLY1 functions in the nucleus to regulate barley leaf development and associated metabolite profiles

Karpińska

Razak

James

et al. 2022

Biochemical Journal

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“…At 10 a.m. of the next day, rosettes of covered plants were harvested. Rosettes were cleared in 80% (v/v) ethanol plus 5% (v/v) formic acid at room temperature, stained in I 2 -KI solution (5 g I 2 and 10 g KI per 100 ml sterile water) and washed three times in water (Huang, et al, 2020).…”

Section: Starch Stainingmentioning

confidence: 99%

“…Semi-qRT-PCR and RT-qPCR analyses employed the oligonucleotide primers described in Supplementary Table S3 and S4. RNA was extracted from rosette leaves of 6-week-old upl3 and wildtype plants, the following procedure was performed according to the description (Huang et al, 2020). Semi-qRT-PCR was performed on an ARKTIK thermal cycler (Thermo Scienti c).…”

Section: Semi-qrt-pcr and Rt-qpcrmentioning

confidence: 99%

“…Full-length or different regions of candidates were cloned into pGADT7-AD vectors to construct prey constructs, and the Bait vector pGBKT7-BD expressed the wild type UPL3 or UPL3 variants fused to the GAL4 DNA binding domain (BD). The procedure was according to the described by Huang et al (2020). The primers were listed in Supplementary Table S2.…”

Section: Yeast Two Hybrid Assaymentioning

confidence: 99%

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Multi-omics analysis reveals a non-canonical regulatory pattern of UPL3 on carbon metabolism related cell senescence

Miao

2022

Preprint

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The HECT domain-containing UPL3 ligase plays critical roles in plant development and stress protection, but its mechanism of action remains limited. To globally identify its targets in Arabidopsis thaliana, we conducted proteomic analyses of ubiquitinated proteins in upl3 mutants via label-free mass spectrometry. In 6-week-old plants, a landscape of UPL3-dependent ubiquitinated proteins is constructed based on correlated datasets of ubiquitome, proteome, and transcriptome. Preferential ubiquitination of proteins related to carbon fixation represented the largest set of proteins with increased ubiquitination in the upl3 plant, while a small set of proteins with reduced ubiquitination caused by the upl3 mutation were linked to cysteine/methionine synthesis and protein translation processes. Furthermore, the upl3 mutation led to an increase in ubiquitination of some of proteins including chromatin remodeling ATPase (BRM), histone proteins, and most of carbon metabolic enzymes, but decreased the ubiquitination of hexokinase 1 (HXK1), phosphoenolpyruvate carboxylase 2 (PPC2), ribosomal protein S5, and H1/H5 domain proteins. Notably, ubiquitin hydrolase 12 (UBP12), BRM, and PPC2 were identified as the UPL3-interacting partners by both GFP-nanotrap-Mass-Spectrometry analyses and yeast two-hybrid assay. Characterization of upl3, brm, and ubp12 mutant plants and transcriptome analysis suggested that UPL3 fine-tunes carbon metabolism mediating cellular senescence by interacting with UBP12, BRM, and PPC2 in the nucleus. Our results highlight an important function of UPL3 as a hub of regulator on proteolysis-independent regulation and proteolysis-dependent degradation.

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WHIRLY protein functions in plants

Taylor

West

Foyer

2022

Food and Energy Security

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Environmental stresses pose a significant threat to food security. Understanding the function of proteins that regulate plant responses to biotic and abiotic stresses is therefore pivotal in developing strategies for crop improvement. The WHIRLY (WHY) family of DNA‐binding proteins are important in this regard because they fulfil a portfolio of important functions in organelles and nuclei. The WHY1 and WHY2 proteins function as transcription factors in the nucleus regulating phytohormone synthesis and associated growth and stress responses, as well as fulfilling crucial roles in DNA and RNA metabolism in plastids and mitochondria. WHY1, WHY2 (and WHY3 proteins in Arabidopsis) maintain organelle genome stability and serve as auxiliary factors for homologous recombination and double‐strand break repair. Our understanding of WHY protein functions has greatly increased in recent years, as has our knowledge of the flexibility of their localization and overlap of functions but there is no review of the topic in the literature. Our aim in this review was therefore to provide a comprehensive overview of the topic, discussing WHY protein functions in nuclei and organelles and highlighting roles in plant development and stress responses. In particular, we consider areas of uncertainty such as the flexible localization of WHY proteins in terms of retrograde signalling connecting mitochondria, plastids, and the nucleus. Moreover, we identify WHY proteins as important targets in plant breeding programmes designed to increase stress tolerance and the sustainability of crop yield in a changing climate.

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Triple-localized WHIRLY2 Influences Leaf Senescence and Silique Development via Carbon Allocation

Abstract: Triple-localized WHIRLY2 plays a vital role in carbon reallocation from maternal tissue to filial tissue through controlling sucrose transporter gene expression.

Cited by 31 publications

References 66 publications

WHIRLY1 functions in the nucleus to regulate barley leaf development and associated metabolite profiles

WHIRLY1 functions in the nucleus to regulate barley leaf development and associated metabolite profiles

Multi-omics analysis reveals a non-canonical regulatory pattern of UPL3 on carbon metabolism related cell senescence

WHIRLY protein functions in plants

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