Regulation of cell divisions and differentiation by <scp>MALE STERILITY</scp>32 is required for anther development in maize

Moon, Jungyoon; Skibbe, David S.; Timofejeva, Ljudmilla; Wang, Rachel; Kelliher, Timothy; Kremling, Karl A.; Walbot, Virginia; Cande, W. Zacheus

doi:10.1111/tpj.12318

Cited by 68 publications

(64 citation statements)

References 27 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…S6). Ms32, the other historical maize mutant with tapetal periclinal divisions (Chaubal et al, 2000) and high expression in the TP (Moon et al, 2013), encodes a protein that falls into clade C along with rice UDT1 and Arabidopsis DYT1 (Fig. 6).…”

Section: Many Bhlh Proteins Are Associated With Tapetal Developmentmentioning

confidence: 99%

“…Mutant analysis demonstrates that several tapetal bHLHs are crucial for (1) pre-meiotic to meiotic stages: Arabidopsis DYSFUNCTIONAL TAPETUM1 (DYT1) Feng et al, 2012), its rice homolog UNDEVELOPED TAPETUM1 (UDT1) (Jung et al, 2005), and the maize homolog, Male Sterility32 (Ms32) (Moon et al, 2013); rice ETERNAL TAPETUM1 (EAT1 -OS04G0599300, also named DELAYED TAPETUM DEGENERATION or DTD) (Niu et al, 2013;Ji et al, 2013); rice TDR INTERACTING PARTNER2 (TIP2 -OS01T0293100; also named bHLH142) (Fu et al, 2014;Ko et al, 2014); Arabidopsis bHLH10, bHLH89 and bHLH91 (Zhu et al, 2015); as well as for (2) meiotic to post-meiotic stages: Arabidopsis ABORTED MICROSPORES (AMS) (Sorensen et al, 2003;Xu et al, 2010Xu et al, , 2014 and its rice homolog TAPETUM DEGENERATION RETARDATION (TDR) (Li et al, 2006;Zhang et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

MS23, a master basic helix-loop-helix factor, regulates the specification and development of tapetum in maize

et al. 2016

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Section: Many Bhlh Proteins Are Associated With Tapetal Developmentmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

MS23, a master basic helix-loop-helix factor, regulates the specification and development of tapetum in maize

et al. 2016

Self Cite

View full text Add to dashboard Cite

show abstract

“…With advances of forward and reverse genetics, some male-sterile genes have been isolated in maize, such as MALE STERILE CONVERTED ANTHER1 (Chaubal et al, 2003), MULTIPLE ARCHESPORIAL CELLS1 (Wang et al, 2012), MALE STERILITY32 (MS32; Moon et al, 2013), MS8 , AMEIOTIC1 (Pawlowski et al, 2009), ABSENCE OF FIRST DIVISION1 (Golubovskaya et al, 2006), RECOMBINATION PROTEIN51 (Li et al, 2007), MS26 (Albertsen et al, 2006), and MS45 (Albertsen et al, 1993). Only MS26 and MS45 are required for pollen wall development, but their detailed functions have not been confirmed.…”

mentioning

confidence: 99%

IRREGULAR POLLEN EXINE1 Is a Novel Factor in Anther Cuticle and Pollen Exine Formation

et al. 2016

View full text Add to dashboard Cite

ORCID IDs: 0000-0002-4656-3189 (H.S.); 0000-0003-0518-5924 (C.Z.); 0000-0001-9320-9628 (W.J.).Anther cuticle and pollen exine are protective barriers for pollen development and fertilization. Despite that several regulators have been identified for anther cuticle and pollen exine development in rice (Oryza sativa) and Arabidopsis (Arabidopsis thaliana), few genes have been characterized in maize (Zea mays) and the underlying regulatory mechanism remains elusive. Here, we report a novel male-sterile mutant in maize, irregular pollen exine1 (ipe1), which exhibited a glossy outer anther surface, abnormal Ubisch bodies, and defective pollen exine. Using map-based cloning, the IPE1 gene was isolated as a putative glucose-methanolcholine oxidoreductase targeted to the endoplasmic reticulum. Transcripts of IPE1 were preferentially accumulated in the tapetum during the tetrad and early uninucleate microspore stage. A biochemical assay indicated that ipe1 anthers had altered constituents of wax and a significant reduction of cutin monomers and fatty acids. RNA sequencing data revealed that genes implicated in wax and flavonoid metabolism, fatty acid synthesis, and elongation were differentially expressed in ipe1 mutant anthers. In addition, the analysis of transfer DNA insertional lines of the orthologous gene in Arabidopsis suggested that IPE1 and their orthologs have a partially conserved function in male organ development. Our results showed that IPE1 participates in the putative oxidative pathway of C16/C18 v-hydroxy fatty acids and controls anther cuticle and pollen exine development together with MALE STERILITY26 and MALE STERILITY45 in maize.Male sterility is a common biological phenomenon in plants and widely used in the production of hybrid seeds, which can reduce costs and enhance seed purity (Tester and Langridge, 2010). According to inheritance or origin, male sterility includes three types: genic male sterility, cytoplasmic male sterility, and cytoplasmicgenic male sterility (Rhee et al., 2015). The generation of mature pollen grains relies on anther development. The start of anther formation occurs in differentiated flower tissues (floral meristem), which consist of three histogenic layers: L1, L2, and L3. After continuous cell division and differentiation, L1 forms the epidermis and the L3 layer develops into the stomium and vascular bundles. L2 is the most important layer; it undergoes a series of periclinal and anticlinal divisions and eventually grows into the endothecium, the middle layer, the tapetum, and the pollen mother cells. When anther morphogenesis is completed, the anther has centrally localized pollen mother cells enclosed by four somatic layers, which are, from the surface to the interior, the epidermis, endothecium, middle layer, and tapetum. Then, the pollen mother cells undergo meiosis and mitosis, resulting in trinucleate pollen grains, and the endothecium, middle layer, and tapetum are gradually degraded (Goldberg et al., 1993(Goldberg et al., , 1995Ma, 2005).The anther cuticle and poll...

show abstract

“…To date, only four male sterility genes, ms31, ms32, ms38, and ms33, are reported to map to the long arm of chromosome 2 (Supplemental Table 2; Trimnell et al 1998;Albertsen et al 1999;Trimnell et al 1999;Skibbe & Schnable 2005). The five male sterility genes had never been sequenced or cloned with the exception of ms32, which coded a basic helixÀ loopÀhelix (bHLH) transcription factor involved in the regulation of early anther development (Chaubal et al 2000;Vernoud et al 2009;Moon et al 2013). However, ms32, which is located in the 2.08 bin, is upstream from the SSR mapping front marker bnlg1940.…”

Section: Discussionmentioning

confidence: 99%

Characterization and genetic mapping of a novel recessive genic male sterile gene ms305 in maize (Zea mays L.)

Wang¹,

Gu²,

Chen³

et al. 2015

Israel Journal of Plant Sciences

View full text Add to dashboard Cite

The male sterility system shows tremendous value for the long-term utilization of hybrid crop breeding. In this study, a male sterile mutant, K305ms, was derived from the M3 progeny of maize (Zea mays L.) inbred line K305 exposed to 60Co-γ irradiation. Male sterile K305ms plants did not show any obvious differences from their sibling male fertile plants (K305F) during the vegetative stage, but failed to produce functional pollen at the reproductive stage. Microscopic observations determined that the dyads and tetrads from the pollen of K305ms plants developed abnormally, and subsequently the microspores were shriveled. Genetic analysis indicated that the male sterility of K305ms was controlled by a single recessive genic gene. Gene mapping showed that the responsible gene was located between two simple sequence repeat markers on chromosome 2L in a region of 10.3 cM, bnlg469b and bnlg1940, with genetic distances of 2.9 and 7.4 cM, respectively. According to the microscopic and mapping characteristics, our results showed that this gene was distinguishable from all other reported male sterile genes in maize, and it is temporarily designated as ms305. The linkage map in this study will provide a useful fundamental basis for molecular marker-assisted selection as well as for further map-based cloning of ms305.

show abstract

Regulation of cell divisions and differentiation by MALE STERILITY32 is required for anther development in maize

Cited by 68 publications

References 27 publications

MS23, a master basic helix-loop-helix factor, regulates the specification and development of tapetum in maize

MS23, a master basic helix-loop-helix factor, regulates the specification and development of tapetum in maize

IRREGULAR POLLEN EXINE1 Is a Novel Factor in Anther Cuticle and Pollen Exine Formation

Characterization and genetic mapping of a novel recessive genic male sterile gene ms305 in maize (Zea mays L.)

Contact Info

Product

Resources

About