PIF4 negatively modulates cold tolerance in tomato anthers via temperature-dependent regulation of tapetal cell death

Pan, Changtian; Yang, Dandan; Zhao, Xiaolin; Liu, Yue; Li, Mengzhuo; Ye, Lei; Ali, Muhammad; Yu, Fangjie; Lamin-Samu, Anthony Tumbeh; Fei, Zhangjun; Lü, Gang

doi:10.1093/plcell/koab120

Cited by 35 publications

(28 citation statements)

References 109 publications

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“…The empty vector of pVBG2307:GFP was used as a control check. Four-week-old tobacco plantlets expressing the red nuclear marker RFP-H2B were agroinfiltrated and then placed in a growth chamber for 2–3 days [ 57 ]. Localized protein expression was scanned with an Olympus BX63 automated fluorescence microscope (Olympus, Tokyo, Japan).…”

Section: Methodsmentioning

confidence: 99%

Mitogen-activated protein kinase 4 is obligatory for late pollen and early fruit development in tomato

Wang

Zhuo

et al. 2022

Horticulture Research

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Mitogen-activated protein kinase (MPK) cascades are universal signal transduction modules regulating vegetative and reproductive development of plants. However, the molecular mechanisms of SlMPK4 gene in tomato pollen and fruit development remain elusive. SlMPK4 is preferentially and highly expressed in tomato stamens and its mRNA levels increase during early flower development, peaking at the mature pollen stage. Either up- or down-regulation of SlMPK4 expression had no significant effect on tomato vegetative growth. Though, RNAi-mediated suppression of SlMPK4 caused defects in pollen development, resulting in pollen abortion. The aborted pollen grains were either malformed or collapsed and completely lacked viability, resulting in predominately reduced fruit set rate in RNAi lines compared with control and overexpressed transgenic plants. Interestingly, the seed development was inhibited in RNAi-lines. Moreover, >12% of emasculated RNAi flowers developed seedless fruits without pollination. Anthers can produce typical microspore mother cells (MMCs) as well as uninucleate microspores, according to cytological investigations, while binucleate pollen ceased to produce typical mature pollen. The pollen abortion was further confirmed by transmission electron microscopy (TEM) analysis at binucleate stage in RNAi plants. The exine layer in aberrant pollen had a normal structure, while the intine layer appeared thicker. Suppression of SlMPK4 affects the transcript level of cell wall formation and modification, cell signal transduction, and metabolic and biosynthetic processes related genes. A subset of genes which may be putative substrates of plant MAPKs were also differentially changed in RNAi transgenic flowers. Taken together, these results suggest that SlMPK4 plays a critical role in regulating pollen development and fruit development in tomato plants.

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Section: Methodsmentioning

confidence: 99%

Mitogen-activated protein kinase 4 is obligatory for late pollen and early fruit development in tomato

Wang

Zhuo

et al. 2022

Horticulture Research

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“…2c ), consistent with its roles at PMI. This situation is different from other bHLH family members, such as AMS and DYT1 from A. thaliana , TDR and EAT1 from rice and SlPIF4 from tomato, which are all involved in pollen development by regulating tapetum development (Sorensen et al ., 2003 ; Zhang et al ., 2006 ; Zhu et al ., 2015 ; Pan et al ., 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…Here, 295‐bp SlPIF3 , 239‐bp SlGLT1 and 275‐bp SlCWIN9 coding sequence (CDS) fragments were each amplified and used as templates for transcription with SP6 and T7 RNA polymerases to produce digoxigenin‐labelled RNA probes (Roche, Germany). SlPIF3 subcellular localisation was performed as previously reported (Pan et al ., 2021 ). The primers used are listed in Dataset S1 .…”

Section: Methodsmentioning

confidence: 99%

“…For example, Arabidopsis PIF4 is a central hub regulator involving auxin biosynthesis and signalling to promote hypocotyl and petiole elongation (Hornitschek et al ., 2012 ); PIF5 acts as a master switch in sugar‐induced auxin biosynthesis in A. thaliana seedlings (Sairanen et al ., 2013 ). Recently, our group demonstrated that SlPIF4 plays an essential role in regulating the adaptation of tomato pollen development to low temperature stress via anther tapetal cell death (Pan et al ., 2021 ). According to our previously published transcriptome data, SlPIF3 and SlPIF4 are highly expressed in tomato anthers (Chen et al ., 2018 ; Pan et al ., 2019 ).…”

Section: Introductionmentioning

confidence: 99%

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Phytochrome interacting factor 3 regulates pollen mitotic division through auxin signalling and sugar metabolism pathways in tomato

et al. 2021

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The development of viable pollen determines male fertility, and is crucial for reproduction in flowering plants. Phytochrome interacting factor 3 (PIF3) acts as a central regulator of plant growth and development, but its relationship with pollen development has not been determined.Through genetic, histological and transcriptomic analyses, we identified an essential role for SlPIF3 in regulating tomato (Solanum lycopersicum) pollen development. Knocking out SlPIF3 using clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 resulted in pollen mitosis I arrest, and a failure to form viable pollen. We further demonstrated that both glutamate synthase 1 (SlGLT1) and cell wall invertase 9 (SlCWIN9), involved in auxin and sugar homeostasis, respectively, colocalised with SlPIF3 in the anthers and were directly regulated by SlPIF3. Knockout of either SlGLT1 or SlCWIN9 phenocopied the pollen phenotype of SlPIF3 knockout (Slpif3) lines.Slpif3 fertility was partially restored by exogenous auxin indole-3-acetic acid in a dosedependent manner.This study reveals a mechanism by which SlPIF3 regulates pollen development and highlights a new strategy for creating hormone-regulated genic male sterile lines for tomato hybrid seed production.

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“…Notably, a substantial increase in the number of bHLH proteins has been demonstrated to play an important role in the response to abiotic stresses, including cold, drought, and salt stress. For example, in tomatoes, SlPIF4 modulates cold tolerance in anthers via the temperature-dependent regulation of tapetal cell death ( Pan et al, 2021 ). In rice, OsbHLH148 regulates drought tolerance via jasmonic acid signaling pathway ( Seo et al, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

Genome-Wide Characterization and Analysis of the bHLH Transcription Factor Family in Suaeda aralocaspica, an Annual Halophyte With Single-Cell C4 Anatomy

2022

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Basic helix-loop-helix (bHLH) transcription factors play important roles in plant growth, development, metabolism, hormone signaling pathways, and responses to abiotic stresses. However, comprehensive genomic and functional analyses of bHLH genes have not yet been reported in desert euhalophytes. Suaeda aralocaspica, an annual C4 halophyte without Kranz anatomy, presents high photosynthetic efficiency in harsh natural habitats and is an ideal plant for identifying transcription factors involved in stress resistance. In this study, 83 bHLH genes in S. aralocaspica were identified and categorized into 21 subfamilies based on conserved motifs, gene structures, and phylogenetic analysis. Functional annotation enrichment revealed that the majority of SabHLHs were enriched in Gene Ontology (GO) terms and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways involved in the response to stress conditions, as transcription factors. A number of cis-acting elements related to plant hormones and stress responses were also predicted in the promoter regions of SabHLHs, which were confirmed by expression analysis under various abiotic stress conditions (NaCl, mannitol, low temperature, ABA, GA3, MeJA, and SA); most were involved in tolerance to drought and salinity. SabHLH169 (076) protein localized in the nucleus was involved in transcriptional activity, and gene expression could be affected by different light qualities. This study is the first comprehensive analysis of the bHLH gene family in S. aralocaspica. These data will facilitate further characterization of their molecular functions in the adaptation of desert plants to abiotic stress.

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PIF4 negatively modulates cold tolerance in tomato anthers via temperature-dependent regulation of tapetal cell death

Cited by 35 publications

References 109 publications

Mitogen-activated protein kinase 4 is obligatory for late pollen and early fruit development in tomato

Mitogen-activated protein kinase 4 is obligatory for late pollen and early fruit development in tomato

Phytochrome interacting factor 3 regulates pollen mitotic division through auxin signalling and sugar metabolism pathways in tomato

Genome-Wide Characterization and Analysis of the bHLH Transcription Factor Family in Suaeda aralocaspica, an Annual Halophyte With Single-Cell C4 Anatomy

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