Heat shock protein 101 contributes to the thermotolerance of male meiosis in maize

Li, Yunfei; Huang, Yuxin; Sun, Huayue; Wang, Tianyi; Ru, Wei; Pan, Lingling; Zhao, Xiaoming; Dong, Zhaobin; Huang, Wei; Jin, Weiwei

doi:10.1093/plcell/koac184

Cited by 15 publications

(10 citation statements)

References 83 publications

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“…It is only recently that the genetic basis of these heat induced defects is being elucidated in plants. Examples include the sporophitically expressed unfolded protein response component IRE1 (Deng et al 2016), MAGO1 and MAGO2 that function in meiocyte initials in a transposon surveillance mechanism (Lee et al 2021) or the role of HSP101 in proper loading of RAD51 (Li et al 2022). By exploiting the natural variation in Arabidopsis we here uncovered TAM as a major molecular player in heat induced meiotic restitution.…”

Section: Discussionmentioning

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: Discussionmentioning

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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“…The meiotic chromosome preparation and immunofluorescence staining procedures were performed as described previously (Li et al ., 2022). The polyclonal antibody against ZEP1 (Wang et al ., 2010) and monoclonal antibody against α‐tubulin (ab7750; Abcam, Cambridge, UK) were raised in mouse, and polyclonal antibodies against γH2AX and AFD1 (Li et al ., 2022) were raised in rabbit. Fluorescein‐5‐isothiocyanate‐conjugated goat anti‐mouse and Alexa Fluor 647‐conjugated goat anti‐rabbit antibodies were purchased from Abclonal (Wuhan, China).…”

Section: Methodsmentioning

confidence: 99%

“…Quantitative reverse transcription PCR (RT‐qPCR) was performed to determine the relative expression level of invan6 in vegetative organs (root, leaf, stem) of V5 plant, meiotic tassel, anthers, and immature seeds (3 and 6 d after pollination). The RNA extraction, reverse transcription, and RT‐qPCR were performed according to previously described protocols (Li et al ., 2022).…”

Section: Methodsmentioning

confidence: 99%

“…One classical gene is Cyclin‐Dependent Kinase G1 , which regulates meiotic chromosome recombination and synapsis in a temperature‐dependent manner in Arabidopsis (Zheng et al ., 2014; Nibau et al ., 2020). And a recent study in maize ( Zea mays ) revealed that Heat Shock Protein 101 is essential for DSB repair and subsequent meiosis under heat stress (Li et al ., 2022). To gain more insights into the interaction between heat stress and male meiosis, it is vital to characterize more key elements that regulate thermotolerance of meiosis.…”

Section: Introductionmentioning

confidence: 99%

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Maize cytosolic invertase INVAN6 ensures faithful meiotic progression under heat stress

Huang

et al. 2022

New Phytologist

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Summary Faithful meiotic progression ensures the generation of viable gametes. Studies suggested the male meiosis of plants is sensitive to ambient temperature, but the underlying molecular mechanisms remain elusive. Here, we characterized a maize (Zea mays ssp. mays L.) dominant male sterile mutant Mei025, in which the meiotic process of pollen mother cells (PMCs) was arrested after pachytene. An Asp‐to‐Asn replacement at position 276 of INVERTASE ALKALINE NEUTRAL 6 (INVAN6), a cytosolic invertase (CIN) that predominantly exists in PMCs and specifically hydrolyses sucrose, was revealed to cause meiotic defects in Mei025. INVAN6 interacts with itself as well as with four other CINs and seven 14‐3‐3 proteins. Although INVAN6Mei025, the variant of INVAN6 found in Mei025, lacks hydrolytic activity entirely, its presence is deleterious to male meiosis, possibly in a dominant negative repression manner through interacting with its partner proteins. Notably, heat stress aggravated meiotic defects in invan6 null mutant. Further transcriptome data suggest INVAN6 has a fundamental role for sugar homeostasis and stress tolerance of male meiocytes. In summary, this work uncovered the function of maize CIN in male meiosis and revealed the role of CIN‐mediated sugar metabolism and signalling in meiotic progression under heat stress.

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“…In rice, the GROWTH REGULATING FACTOR 4 (OsGRF4), and HEAT SHOCK FACTOR60-3B (OsHSP60-3B) are required to secure viability and seed-setting rate under heat stress (Mo et al 2023;Lin et al 2023). And in maize, improved tolerance of meiosis to heat stress has been reported in lines overexpressing HEAT SHOCK PROTEIN101 (HSP101) (Li et al 2022).…”

Section: Heat Oversensitivity Of Rrb1 Pollenmentioning

confidence: 99%

Ribosome biogenesis factor AtRRB1 confers pollen heat stress tolerance in Arabidopsis

Jin,

Schindfessel,

Sun

et al. 2024

Preprint

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The plant male reproductive system is very sensitive to high temperature stress leading to a reduction in fertility. Damage caused by heat stress is restored by the activation of transcription and the synthesis of chaperones that regulate the heat stress response. Here we report that AtRRB1 is a homolog of the yeast ribosome chaperone protein Rrb1p. AtRRB1 is an essential gene and a T-DNA insertion in the coding region impairs male and female gametogenesis. The heterozygous rrb1-1 mutant shows decreased expression of AtRRB1 and increased transcription of the 60S ribosome proteins RPL3B and RPL4, in line with a chaperone role of AtRRB1 in ribosome biogenesis. Embryo sac development across ovules of a single pistil occurs uncoordinated and about half of the ovules abort. Half of rrb1-1 pollen is substantially smaller and produce shorter pollen tubes than WT pollen. In contrast to the Col-0 pollen, smaller pollen is overly sensitivity to high temperature (24h at 32∘C) treatment, specifically during the early bicellular microspore development stage. Heat stressed rrb1-1 bicellular microspores accumulated excessively rough endoplasmic reticulum stacks, suggesting that loss of AtRRB1 activity causes an arrest in ER associated protein biosynthesis. These findings support a critical requirement for ribosome biogenesis and protein synthesis in bicellular microspores to recover from high temperature stress.

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Heat shock protein 101 contributes to the thermotolerance of male meiosis in maize

Cited by 15 publications

References 83 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

Maize cytosolic invertase INVAN6 ensures faithful meiotic progression under heat stress

Ribosome biogenesis factor AtRRB1 confers pollen heat stress tolerance in Arabidopsis

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