A framework for evaluating developmental defects at the cellular level: An example from ten maize anther mutants using morphological and molecular data
Abstract:In seed plants, anthers are critical for sexual reproduction, because they foster both meiosis and subsequent pollen development of male germinal cells. Male-sterile mutants are analyzed to define steps in anther development. Historically the major topics in these studies are meiotic arrest and post-meiotic gametophyte failure, while relatively few studies focus on pre-meiotic defects of anther somatic cells. Utilizing morphometric analysis we demonstrate that pre-meiotic mutants can be impaired in anticlinal … Show more
“…A relatively large size, the 30-day-long period of anther development, and the regularity of ontogeny in which anther length allows accurate developmental staging have facilitated dissection and confocal reconstruction of cell division and expansion patterns in maize anthers (Kelliher and Walbot, 2011). Additionally, there are hundreds of male-sterile mutants (Skibbe and Schnable, 2005) including a subset disrupting somatic lobe development prior to meiosis Egger and Walbot, 2016). These maize resources were developed in part to facilitate hybrid seed production using male-sterile plants as ear parents with pollen supplied by a male-fertile partner line.…”
Successful male gametogenesis involves orchestration of sequential gene regulation for somatic differentiation in pre-meiotic anthers. We report here the cloning of Male Sterile23 (Ms23), encoding an antherspecific predicted basic helix-loop-helix (bHLH) transcription factor required for tapetal differentiation; transcripts localize initially to the precursor secondary parietal cells then predominantly to daughter tapetal cells. In knockout ms23-ref mutant anthers, five instead of the normal four wall layers are observed. Microarray transcript profiling demonstrates a more severe developmental disruption in ms23-ref than in ms32 anthers, which possess a different bHLH defect. RNA-seq and proteomics data together with yeast two-hybrid assays suggest that MS23 along with MS32, bHLH122 and bHLH51 act sequentially as either homo-or heterodimers to choreograph tapetal development. Among them, MS23 is the earliest-acting factor, upstream of bHLH51 and bHLH122, controlling tapetal specification and maturation. By contrast, MS32 is constitutive and independently regulated and is required later than MS23 in tapetal differentiation.
“…A relatively large size, the 30-day-long period of anther development, and the regularity of ontogeny in which anther length allows accurate developmental staging have facilitated dissection and confocal reconstruction of cell division and expansion patterns in maize anthers (Kelliher and Walbot, 2011). Additionally, there are hundreds of male-sterile mutants (Skibbe and Schnable, 2005) including a subset disrupting somatic lobe development prior to meiosis Egger and Walbot, 2016). These maize resources were developed in part to facilitate hybrid seed production using male-sterile plants as ear parents with pollen supplied by a male-fertile partner line.…”
Successful male gametogenesis involves orchestration of sequential gene regulation for somatic differentiation in pre-meiotic anthers. We report here the cloning of Male Sterile23 (Ms23), encoding an antherspecific predicted basic helix-loop-helix (bHLH) transcription factor required for tapetal differentiation; transcripts localize initially to the precursor secondary parietal cells then predominantly to daughter tapetal cells. In knockout ms23-ref mutant anthers, five instead of the normal four wall layers are observed. Microarray transcript profiling demonstrates a more severe developmental disruption in ms23-ref than in ms32 anthers, which possess a different bHLH defect. RNA-seq and proteomics data together with yeast two-hybrid assays suggest that MS23 along with MS32, bHLH122 and bHLH51 act sequentially as either homo-or heterodimers to choreograph tapetal development. Among them, MS23 is the earliest-acting factor, upstream of bHLH51 and bHLH122, controlling tapetal specification and maturation. By contrast, MS32 is constitutive and independently regulated and is required later than MS23 in tapetal differentiation.
“…As for the anther, a host of genes have been known to be involved in its development (Ma, 2005;Egger and Walbot, 2016). Among them, only a few genes function in specifying archesporial cell fate and/or delineating archesporial and somatic cells.…”
Section: Possible Molecular Genetic Mechanisms By Which the Grf-gif Dmentioning
confidence: 99%
“…Each lobe internally develops a microsporangium that consists of three outer concentric parietal layers (i.e. endothecium, middle layer, and tapetum), and the microsporangium harbors pollen mother cells (PMCs; Sanders et al, 1999;Egger and Walbot, 2016;Supplemental Fig. S1).…”
We investigated the biological roles of the Arabidopsis (Arabidopsis thaliana) GROWTH-REGULATING FACTOR (GRF) and GRF-INTERACTING FACTOR (GIF) transcriptional complex in the development of gynoecia and anthers. There are nine GRFs and three GIFs in Arabidopsis, and seven GRFs are posttranscriptionally silenced by microRNA396 (miR396). We found that overexpression of MIR396 in the gif1 gif2 double mutant background (gif1 gif2 35S:MIR396) resulted in neither ovary nor pollen. Histological and molecular marker-based analyses revealed that the mutant gynoecial primordia failed to develop carpel margin meristems and mature flowers lacked the ovary, consisting only of the stigma, style, and replum-like tissues. The mutant anther primordia were not able to form the pluripotent archesporial cells that produce pollen mother cells and microsporangia. Multiple combinations of GRF mutations also displayed the same phenotypes, indicating that the GRF-GIF duo is required for the formation of those meristematic and pluripotent cells. Most GRF proteins are localized and abundant in those cells. We also found that the weak gynoecial defects of pinoid-3 (pid-3) mutants were remarkably exacerbated by gif1 gif2 double mutations and 35S:MIR396, so that none of the gynoecia produced by gif1 gif2 pid-3 and 35S:MIR396 pid-3 developed ovaries at all. Moreover, gif1 gif2 double mutations and 35S:MIR396 also acted synergistically with 1-N-naphthylphthalamic acid in forming aberrant gynoecia. The results altogether suggest that the GRF-GIF duo regulates the meristematic and pluripotent competence of carpel margin meristems and the archesporial cell lineage and that this regulation is implemented in association with auxin action, ultimately conferring reproductive competence on Arabidopsis.
“…Nonetheless, highly regulated cell divisions underlie plant morphogenesis and organogenesis. Egger and Walbot (Egger and Walbot, 2016) provide "a framework for evaluating developmental defects at the cellular level". In this sweeping survey of 24 pre-meiotic male sterile mutants in maize, confocal microscopy is used to analyze the role of cell proliferation defects and cell morphology in producing defined cell layers of the maize anther lobes.…”
Section: A Cellular Basis For Plant Developmental Biologymentioning
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