Specification of female germline by microRNA orchestrated auxin signaling in Arabidopsis

Huang, Jian; Zhao, Lei; Malik, Shikha; Gentile, Benjamin R.; Xiong, Va; Arazi, Tzahi; Owen, Heather A.; Friml, Jiřı́; Zhao, Dazun

doi:10.1038/s41467-022-34723-6

Cited by 13 publications

(11 citation statements)

References 68 publications

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“…Compared with the 3‐day heat‐treated plants, the application of IAA–lanolin mixtures at concentrations of both 0.1 and 10 mg/g at the top of the first internode (the primary panicle was decapitated before treatment) significantly increased the number of apical tillers (Figure 7a–c,f). The polar auxin transporter inhibitor N‐1‐Naphthylphthalamic acid (NPA; Abas et al, 2021; Huang et al, 2022) appears to hinder the apical tiller formation, although not to a statistically significant extent (Figure 7a,d–f). It is noteworthy that treatment with the 10 mg/g of IAA–lanolin mixture significantly increased the leaf number per newly formed apical tiller, while the leaf number per apical tiller was significantly reduced when treated with the 10 mg/g of NPA–lanolin mixture (Figure 7g).…”

Section: Resultsmentioning

confidence: 99%

“…These results suggest that heat stress likely stimulates the apical tiller formation via affecting auxin biosynthesis or auxin signaling at the apex of sorghum. Notably, the application of the polar auxin transporter inhibitor NPA (Abas et al, 2021; Huang et al, 2022) seems to restrain the apical tiller formation, though not reaching statistical significance. It is possible that the plants could not efficiently absorb the NPA, prompting consideration of potential NPA injection into the plants for future experimentation.…”

Section: Discussionmentioning

confidence: 99%

“…To study the effects of heat stress on anther development, semi-thin sectioning was carried out essentially as described in our previous studies (Huang et al, 2016(Huang et al, , 2017(Huang et al, , 2022Zhao et al, 2002). Briefly, the heat-treated and untreated spikelets were dissected and fixed in 2.5% of (vol/vol) glutaraldehyde in 0.1 M HEPES (N-2-Hydroxyethyl pipera-zine-N-2-ethanesulfonic acid) buffer (pH 7.2) and 0.02% of TritonX-100 overnight at 4°C.…”

Section: Sample Collection Alexander Pollen Staining and Anther Semi-...mentioning

confidence: 99%

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The effects of heat stress on male reproduction and tillering in Sorghum bicolor

Smith,

Gentile,

Xin

et al. 2023

Food and Energy Security

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Due to global climate change, heat stress is increasingly harming the growth, development, overall biomass, and grain yield of numerous crops. Heat stress impairs pollen development and thus reduces seed set in Sorghum bicolor (L.) Moench; however, the effects of heat stress on anther development at specific stages and tiller formation remain incompletely understood. Here we report that exposure to heat stress [42°C/32°C (day/night)] at pollen mother cell (PMC) and booting stages profoundly disrupts tapetum and pollen development, resulting in a significant decrease in grain yield in sorghum. Sorghum plants subjected to 9 days or less of heat stress at the PMC stage exhibited normal pollen viability, but 12 days of heat stress caused almost complete loss of grain yield and the formation of nonviable pollen grains. Similarly, sorghum plants that were heat‐stressed for 3 days at the booting stage produced few seeds. Further analysis revealed that aberrant tapetum and pollen development contributed to the sterility of pollen in these heat‐stressed plants. Notably, in addition to inhibiting plant height, a 12‐day heat stress at the PMC stage promoted the formation of basal tillers, whereas a 3‐day heat stress at the booting stage stimulated the formation of apical tillers, which helped salvage seed yield under heat stress conditions. Moreover, the application of exogenous auxin promoted the formation of apical tillers and leaf numbers per apical tiller. Collectively, our findings suggest that sorghum is susceptible to heat stress during both early and late anther development, and auxin might be involved in governing the formation of apical tillers.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Sample Collection Alexander Pollen Staining and Anther Semi-...mentioning

confidence: 99%

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The effects of heat stress on male reproduction and tillering in Sorghum bicolor

Smith,

Gentile,

Xin

et al. 2023

Food and Energy Security

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“…Two well‐known primary miRNA processing factors, SE and HYL1 , were identified in the list of BZR1 target genes. We therefore decided to focus on SE , HYL1 , and DCL1 , as the roles of miRNAs in MMC specification were recently reported (Huang et al ., 2022). qRT‐PCR analysis showed that the transcript level of SE , HYL1 , and DCL1 was significantly reduced in sex‐1 sextuple mutant compared with WT (Fig.…”

Section: Resultsmentioning

confidence: 99%

Epigenetic regulation of female germline development through ERECTA signaling pathway

Huang,

Liu,

Chai

et al. 2023

New Phytologist

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Summary Germline development is a key step in sexual reproduction. Sexual plant reproduction begins with the formation of haploid spores by meiosis of megaspore mother cells (MMCs). Although many evidences, directly or indirectly, show that epigenetics plays an important role in MMC specification, how it controls the commitment of the MMC to downstream stages of germline development is still unclear. Electrophoretic mobility shift assay (EMSA), western blot, immunofluorescence, and chromatin immunoprecipitation coupled with quantitative PCR analyses were performed. Genetic interactions between BZR1 transcription factor family and the SWR1‐SDG2‐ER pathway in the control of female germline development were further studied. The present findings showed in Arabidopsis that two epigenetic factors, the chromatin remodeling complex SWI2/SNF2‐RELATED 1 (SWR1) and a writer for H3K4me3 histone modification SET DOMAIN GROUP 2 (SDG2), genetically interact with the ERECTA (ER) receptor kinase signaling pathway and regulate female germline development by restricting the MMC cell fate to a single cell in the ovule primordium and ensure that only that single cell undergoes meiosis and subsequent megaspore degeneration. We also showed that SWR1‐SDG2‐ER signaling module regulates female germline development by promoting the protein accumulation of BZR1 transcription factor family on the promoters of primary miRNA processing factors, HYPONASTIC LEAVES 1 (HYL1), DICER‐LIKE 1 (DCL1), and SERRATE (SE) to activate their expression. Our study elucidated a Gene Regulation Network that provides new insights for understanding how epigenetic factors and receptor kinase signaling pathways function in concert to control female germline development in Arabidopsis.

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“…However, although several regulatory factors for both generations were identified in sexual models (Nakajima, 2018;Hisanaga et al, 2019;Pinto et al, 2019;Lora et al, 2019;Hater et al, 2020;Khanday & Sundaresan, 2021;Kim et al, 2021;Vigneau & Borg, 2021;Y. Li et al, 2021;Cai et al, 2022;Huang et al, 2022;Petrella Ó 2023 The Authors New Phytologist Ó 2023 New Phytologist Foundation New Phytologist (2023) 240: 597-612 597 www.newphytologist.com This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Sanchez-Vera et al, 2022), no clear hookup with natural apomictic systems has emerged yet, except evidence for members of the RNA-directed DNA methylation pathway (Grimanelli, 2012;Selva et al, 2017;Galla et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

TRIMETHYLGUANOSINE SYNTHASE1 mutations decanalize female germline development in Arabidopsis

Siena,

Michaud,

Selles

et al. 2023

New Phytologist

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Summary Here, we report the characterization of a plant RNA methyltransferase, orthologous to yeast trimethylguanosine synthase1 (Tgs1p) and whose downregulation was associated with apomixis in Paspalum grasses. Using phylogenetic analyses and yeast complementation, we determined that land plant genomes all encode a conserved, specific TGS1 protein. Next, we studied the role of TGS1 in female reproduction using reporter lines and loss‐of‐function mutants in Arabidopsis thaliana. pAtTGS1:AtTGS1 reporters showed a dynamic expression pattern. They were highly active in the placenta and ovule primordia at emergence but, subsequently, showed weak signals in the nucellus. Although expressed throughout gametophyte development, activity became restricted to the female gamete and was also detected after fertilization during embryogenesis. TGS1 depletion altered the specification of the precursor cells that give rise to the female gametophytic generation and to the sporophyte, resulting in the formation of a functional aposporous‐like lineage. Our results indicate that TGS1 participates in the mechanisms restricting cell fate acquisition to a single cell at critical transitions throughout the female reproductive lineage and, thus, expand our current knowledge of the mechanisms governing female reproductive fate in plants.

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Specification of female germline by microRNA orchestrated auxin signaling in Arabidopsis

Cited by 13 publications

References 68 publications

The effects of heat stress on male reproduction and tillering in Sorghum bicolor

The effects of heat stress on male reproduction and tillering in Sorghum bicolor

Epigenetic regulation of female germline development through ERECTA signaling pathway

TRIMETHYLGUANOSINE SYNTHASE1 mutations decanalize female germline development in Arabidopsis

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