Epigenetic Regulation of Heat Stress in Plant Male Reproduction

Malik, Shikha; Zhao, Dazun

doi:10.3389/fpls.2022.826473

Cited by 14 publications

(15 citation statements)

References 115 publications

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“…High temperatures are known to modify DNA methylation patterns and plant development (Naydenov et al 2015; Chen et al 2016; Kawakatsu et al 2016; Malik 2022). Data from the 1001 epigenomes project (Kawakatsu et al 2016) revealed that the TAM promotor contains very few DNA methylation marks in leaf material of most accessions at control temperature conditions (Supp.…”

Section: Resultsmentioning

confidence: 99%

Heat stress induces unreduced male gamete formation by targeting the meiotic cyclin TAM/CYCA1;2

Schindfessel

Jin

Geelen

2022

Preprint

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High temperature stress has a profound impact on many aspects of plant development. Particularly male germline development is highly sensitive and has received extensive attention in the light of the ongoing climate change. We here uncover a major role for the cyclin TAM/CYCA1;2 in heat induced male meiotic restitution. By exploiting natural variation in Arabidopsis thaliana we identified rare allelic variants of TAM that confer hypersensitivity to heat stress. The increase of the ambient temperature to 32{degree sign}C for 24 hours is sufficient to stimulate the production of up to 100% unreduced meiocytes, resulting in sexual polyploidisation. Arabidopsis accessions with a heat sensitive TAM allele show elevated expression of TAM at 32oC and overexpression of TAM phenocopies the meiotic restitution phenotype of a TAM knock-out. These results are discussed in terms of the molecular mechanism and indicate a critical role for meiotic cell cycle regulation in sexual polyploidization and plant evolutionary processes.

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Section: Resultsmentioning

confidence: 99%

Heat stress induces unreduced male gamete formation by targeting the meiotic cyclin TAM/CYCA1;2

Schindfessel

Jin

Geelen

2022

Preprint

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“…DNA methylation is an essential epigenetic mechanism for plants at the reproductive stage during HT stress (Malik and Zhao, 2022). Until now in plants, four distinct types of DNA methyltransferases are known, namely (i) MET1 (DNA-methytransferase1), (ii) CMT (chromomethyltransferase), (iii) Dnmt2 (DNA-methyltransferase2) and (iv) DRM (domain rearranged methyltransferase) and four distinct demethylases for catalysing cytosine methylation including (i) DME (Demeter), (ii) DML2 (Demeter like 2), (iii) DML3 (Demeter like 3) and ROS1 (repressor of silencing 1) were found (Malik and Zhao, 2022). During HT stress, various genes are involved in DNA methylation.…”

Section: Epigenetics Involved In Male Sterility During Ht Stressmentioning

confidence: 99%

“…In plants, DNA methylation can be established through the RNA-directed DNA methylation (RdDM) pathway and it requires 24 nucleotide siRNAs (Singh and Prasad, 2022b). In anthers, CHH methylation caused by RdDM is more prominent as compared to CH and CHG methylation and RdDM function is reduced in the initial stages (TS and TDS) of growth as compared to late stages (anther dehiscence stage) during HT stress condition (Ma et al, 2018;Malik and Zhao, 2022). In further studies, during HT stress, Naydenov et al (2015) found the up-regulation of Pol IV and Pol V large subunits, Methylase 1 (MET1), domain rearranged methyltransferase 2 (DRM2) and chromomethlyase 3 (CMT3).…”

Section: Epigenetics Involved In Male Sterility During Ht Stressmentioning

confidence: 99%

High‐temperature stress in crops: male sterility, yield loss and potential remedy approaches

Khan

Ling

et al. 2022

Plant Biotechnology Journal

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Summary Global food security is one of the utmost essential challenges in the 21st century in providing enough food for the growing population while coping with the already stressed environment. High temperature (HT) is one of the main factors affecting plant growth, development and reproduction and causes male sterility in plants. In male reproductive tissues, metabolic changes induced by HT involve carbohydrates, lipids, hormones, epigenetics and reactive oxygen species, leading to male sterility and ultimately reducing yield. Understanding the mechanism and genes involved in these pathways during the HT stress response will provide a new path to improve crops by using molecular breeding and biotechnological approaches. Moreover, this review provides insight into male sterility and integrates this with suggested strategies to enhance crop tolerance under HT stress conditions at the reproductive stage.

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“…The histone proteins H1, H2A, H2B and H3 with the exception of H4 have specialized histone variants that reprogram the gene expression responsible for heat acclimation and heat stress memory. Several key genes and networks regulating the heat response have been identified, and heat stress memory is associated with epigenetic changes ( Li et al., 2021 ; Malik and Zhao, 2022 ). In contrast to hormonal regulation underlying heat stress at the transcriptional level, epigenetic regulation under stress in plants remains elusive, suggesting that identifying key mechanisms is important.…”

Section: Regulation Of Heat Stress In Plantsmentioning

confidence: 99%

Epigenetic stress memory: A new approach to study cold and heat stress responses in plants

Ramakrishnan

Zhang

Mullasseri³

et al. 2022

Front. Plant Sci.

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Understanding plant stress memory under extreme temperatures such as cold and heat could contribute to plant development. Plants employ different types of stress memories, such as somatic, intergenerational and transgenerational, regulated by epigenetic changes such as DNA and histone modifications and microRNAs (miRNA), playing a key role in gene regulation from early development to maturity. In most cases, cold and heat stresses result in short-term epigenetic modifications that can return to baseline modification levels after stress cessation. Nevertheless, some of the modifications may be stable and passed on as stress memory, potentially allowing them to be inherited across generations, whereas some of the modifications are reactivated during sexual reproduction or embryogenesis. Several stress-related genes are involved in stress memory inheritance by turning on and off transcription profiles and epigenetic changes. Vernalization is the best example of somatic stress memory. Changes in the chromatin structure of the Flowering Locus C (FLC) gene, a MADS-box transcription factor (TF), maintain cold stress memory during mitosis. FLC expression suppresses flowering at high levels during winter; and during vernalization, B3 TFs, cold memory cis-acting element and polycomb repressive complex 1 and 2 (PRC1 and 2) silence FLC activation. In contrast, the repression of SQUAMOSA promoter-binding protein-like (SPL) TF and the activation of Heat Shock TF (HSFA2) are required for heat stress memory. However, it is still unclear how stress memory is inherited by offspring, and the integrated view of the regulatory mechanisms of stress memory and mitotic and meiotic heritable changes in plants is still scarce. Thus, in this review, we focus on the epigenetic regulation of stress memory and discuss the application of new technologies in developing epigenetic modifications to improve stress memory.

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Epigenetic Regulation of Heat Stress in Plant Male Reproduction

Cited by 14 publications

References 115 publications

Heat stress induces unreduced male gamete formation by targeting the meiotic cyclin TAM/CYCA1;2

Heat stress induces unreduced male gamete formation by targeting the meiotic cyclin TAM/CYCA1;2

High‐temperature stress in crops: male sterility, yield loss and potential remedy approaches

Epigenetic stress memory: A new approach to study cold and heat stress responses in plants

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