The plant-specific protein FEHLSTART controls male meiotic entry, initializing meiotic synchronization in Arabidopsis

Junhua Li, Stefanie Dukowic-Schulze, Ingrid E. Lindquist, Andrew D. Farmer, Bridget Kelly, Tao Li, Alan G. Smith, Ernest F. Retzel, Joann Mudge, Changbin Chen

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Meiosis marks the transition from the sporophyte to the gametophyte generation in the life cycle of flowering plants, and creates genetic variations through homologous recombination. In most flowering plants, meiosis is highly synchronized within each anther, which is significant for efficient fertilization. To date, little is known about the molecular mechanisms of entry into meiosis and exit from it, and only a few genes in Arabidopsis have been characterized with a role in regulating meiotic progression. In this study, we report the functional characterization of a plant-specific basic helix-loop-helix (bHLH) protein, FEHLSTART (FST), a defect in which leads to premature meiotic entry and asynchronous meiosis, and results in decreased seed yield. Investigation of the time course of meiosis showed that the onset of leptotene, the first stage of prophase I, frequently occurred earlier in fst-1 than in the wild type. Asynchronous meiosis followed, which could manifest in the disruption of regular spindle structures and symmetric cell divisions in fst-1 mutants during the meiosis I/II transition. In accordance with frequently accelerated meiotic entry, whole-transcriptome analysis of fst-1 anthers undergoing meiosis revealed that 19 circadian rhythm genes were affected and 47 pollen-related genes were prematurely expressed at a higher level. Taken together, we propose that FST is required for normal meiotic entry and the establishment of meiotic synchrony. Significance Statement Understanding how plants achieve efficient fertilization is key for plant propagation and crop yield. Here we show that FEHLSTART (FST), a basic helix-loop-helix transcription factor, is required for the synchronous entry into and progression of male meiosis.

Original languageEnglish (US)
Pages (from-to)659-671
Number of pages13
JournalPlant Journal
Volume84
Issue number4
DOIs
StateAccepted/In press - 2015

Fingerprint

Plant Proteins
Meiosis
Arabidopsis
meiosis
proteins
Meiotic Prophase I
Fertilization
anthers
Angiospermae
basic helix-loop-helix transcription factors
Genes
Basic Helix-Loop-Helix Transcription Factors
plant propagation
genes
Homologous Recombination
homologous recombination
prophase
Gene Expression Profiling
Circadian Rhythm
Pollen

Keywords

  • Arabidopsis thaliana
  • FEHLSTART
  • bHLH protein
  • meiosis
  • meiotic entry
  • synchrony

Cite this

Li, J., Dukowic-Schulze, S., Lindquist, I. E., Farmer, A. D., Kelly, B., Li, T., ... Chen, C. (Accepted/In press). The plant-specific protein FEHLSTART controls male meiotic entry, initializing meiotic synchronization in Arabidopsis. Plant Journal, 84(4), 659-671. https://doi.org/10.1111/tpj.13026

The plant-specific protein FEHLSTART controls male meiotic entry, initializing meiotic synchronization in Arabidopsis. / Li, Junhua; Dukowic-Schulze, Stefanie; Lindquist, Ingrid E.; Farmer, Andrew D.; Kelly, Bridget; Li, Tao; Smith, Alan G.; Retzel, Ernest F.; Mudge, Joann; Chen, Changbin.

In: Plant Journal, Vol. 84, No. 4, 2015, p. 659-671.

Research output: Contribution to journalArticle

Li, J, Dukowic-Schulze, S, Lindquist, IE, Farmer, AD, Kelly, B, Li, T, Smith, AG, Retzel, EF, Mudge, J & Chen, C 2015, 'The plant-specific protein FEHLSTART controls male meiotic entry, initializing meiotic synchronization in Arabidopsis', Plant Journal, vol. 84, no. 4, pp. 659-671. https://doi.org/10.1111/tpj.13026
Li, Junhua ; Dukowic-Schulze, Stefanie ; Lindquist, Ingrid E. ; Farmer, Andrew D. ; Kelly, Bridget ; Li, Tao ; Smith, Alan G. ; Retzel, Ernest F. ; Mudge, Joann ; Chen, Changbin. / The plant-specific protein FEHLSTART controls male meiotic entry, initializing meiotic synchronization in Arabidopsis. In: Plant Journal. 2015 ; Vol. 84, No. 4. pp. 659-671.
@article{b3d9d5a58abd4f99aeb60aceeaecdbbf,
title = "The plant-specific protein FEHLSTART controls male meiotic entry, initializing meiotic synchronization in Arabidopsis",
abstract = "Meiosis marks the transition from the sporophyte to the gametophyte generation in the life cycle of flowering plants, and creates genetic variations through homologous recombination. In most flowering plants, meiosis is highly synchronized within each anther, which is significant for efficient fertilization. To date, little is known about the molecular mechanisms of entry into meiosis and exit from it, and only a few genes in Arabidopsis have been characterized with a role in regulating meiotic progression. In this study, we report the functional characterization of a plant-specific basic helix-loop-helix (bHLH) protein, FEHLSTART (FST), a defect in which leads to premature meiotic entry and asynchronous meiosis, and results in decreased seed yield. Investigation of the time course of meiosis showed that the onset of leptotene, the first stage of prophase I, frequently occurred earlier in fst-1 than in the wild type. Asynchronous meiosis followed, which could manifest in the disruption of regular spindle structures and symmetric cell divisions in fst-1 mutants during the meiosis I/II transition. In accordance with frequently accelerated meiotic entry, whole-transcriptome analysis of fst-1 anthers undergoing meiosis revealed that 19 circadian rhythm genes were affected and 47 pollen-related genes were prematurely expressed at a higher level. Taken together, we propose that FST is required for normal meiotic entry and the establishment of meiotic synchrony. Significance Statement Understanding how plants achieve efficient fertilization is key for plant propagation and crop yield. Here we show that FEHLSTART (FST), a basic helix-loop-helix transcription factor, is required for the synchronous entry into and progression of male meiosis.",
keywords = "Arabidopsis thaliana, FEHLSTART, bHLH protein, meiosis, meiotic entry, synchrony",
author = "Junhua Li and Stefanie Dukowic-Schulze and Lindquist, {Ingrid E.} and Farmer, {Andrew D.} and Bridget Kelly and Tao Li and Smith, {Alan G.} and Retzel, {Ernest F.} and Joann Mudge and Changbin Chen",
year = "2015",
doi = "10.1111/tpj.13026",
language = "English (US)",
volume = "84",
pages = "659--671",
journal = "Plant Journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell",
number = "4",

}

TY - JOUR

T1 - The plant-specific protein FEHLSTART controls male meiotic entry, initializing meiotic synchronization in Arabidopsis

AU - Li, Junhua

AU - Dukowic-Schulze, Stefanie

AU - Lindquist, Ingrid E.

AU - Farmer, Andrew D.

AU - Kelly, Bridget

AU - Li, Tao

AU - Smith, Alan G.

AU - Retzel, Ernest F.

AU - Mudge, Joann

AU - Chen, Changbin

PY - 2015

Y1 - 2015

N2 - Meiosis marks the transition from the sporophyte to the gametophyte generation in the life cycle of flowering plants, and creates genetic variations through homologous recombination. In most flowering plants, meiosis is highly synchronized within each anther, which is significant for efficient fertilization. To date, little is known about the molecular mechanisms of entry into meiosis and exit from it, and only a few genes in Arabidopsis have been characterized with a role in regulating meiotic progression. In this study, we report the functional characterization of a plant-specific basic helix-loop-helix (bHLH) protein, FEHLSTART (FST), a defect in which leads to premature meiotic entry and asynchronous meiosis, and results in decreased seed yield. Investigation of the time course of meiosis showed that the onset of leptotene, the first stage of prophase I, frequently occurred earlier in fst-1 than in the wild type. Asynchronous meiosis followed, which could manifest in the disruption of regular spindle structures and symmetric cell divisions in fst-1 mutants during the meiosis I/II transition. In accordance with frequently accelerated meiotic entry, whole-transcriptome analysis of fst-1 anthers undergoing meiosis revealed that 19 circadian rhythm genes were affected and 47 pollen-related genes were prematurely expressed at a higher level. Taken together, we propose that FST is required for normal meiotic entry and the establishment of meiotic synchrony. Significance Statement Understanding how plants achieve efficient fertilization is key for plant propagation and crop yield. Here we show that FEHLSTART (FST), a basic helix-loop-helix transcription factor, is required for the synchronous entry into and progression of male meiosis.

AB - Meiosis marks the transition from the sporophyte to the gametophyte generation in the life cycle of flowering plants, and creates genetic variations through homologous recombination. In most flowering plants, meiosis is highly synchronized within each anther, which is significant for efficient fertilization. To date, little is known about the molecular mechanisms of entry into meiosis and exit from it, and only a few genes in Arabidopsis have been characterized with a role in regulating meiotic progression. In this study, we report the functional characterization of a plant-specific basic helix-loop-helix (bHLH) protein, FEHLSTART (FST), a defect in which leads to premature meiotic entry and asynchronous meiosis, and results in decreased seed yield. Investigation of the time course of meiosis showed that the onset of leptotene, the first stage of prophase I, frequently occurred earlier in fst-1 than in the wild type. Asynchronous meiosis followed, which could manifest in the disruption of regular spindle structures and symmetric cell divisions in fst-1 mutants during the meiosis I/II transition. In accordance with frequently accelerated meiotic entry, whole-transcriptome analysis of fst-1 anthers undergoing meiosis revealed that 19 circadian rhythm genes were affected and 47 pollen-related genes were prematurely expressed at a higher level. Taken together, we propose that FST is required for normal meiotic entry and the establishment of meiotic synchrony. Significance Statement Understanding how plants achieve efficient fertilization is key for plant propagation and crop yield. Here we show that FEHLSTART (FST), a basic helix-loop-helix transcription factor, is required for the synchronous entry into and progression of male meiosis.

KW - Arabidopsis thaliana

KW - FEHLSTART

KW - bHLH protein

KW - meiosis

KW - meiotic entry

KW - synchrony

UR - http://www.scopus.com/inward/record.url?scp=84955170922&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84955170922&partnerID=8YFLogxK

U2 - 10.1111/tpj.13026

DO - 10.1111/tpj.13026

M3 - Article

C2 - 26382719

AN - SCOPUS:84955170922

VL - 84

SP - 659

EP - 671

JO - Plant Journal

JF - Plant Journal

SN - 0960-7412

IS - 4

ER -