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The wheat AGL6-like MADS-box gene is a master regulator for floral organ identity and a target for spikelet meristem development manipulation.

ABSTRACT: The AGAMOUS-LIKE6 (AGL6)-like genes are ancient MADS-box genes and are functionally studied in a few model plants. The knowledge of these genes in wheat remains limited. Here, by studying a 'double homoeolog mutant' of the AGL6 gene in tetraploid wheat, we showed that AGL6 was required for the development of all four whorls of floral organs with dosage-dependent effect on floret fertility. Yeast two-hybrid analyses detected interactions of AGL6 with all classes of MADS-box proteins in the ABCDE model for floral organ development. AGL6 was found to interact with several additional proteins, including the G protein β and γ (DEP1) subunits. Analysis of the DEP1-B mutant showed a significant reduction in spikelet number per spike in tetraploid wheat, while overexpression of AGL6 in common wheat increased the spikelet number per spike and hence the grain number per spike. RNA-seq analysis identified the regulation of several meristem activity genes by AGL6, such as FUL2 and TaMADS55. Our work therefore extensively updated the wheat ABCDE model and proposed an alternative approach to improve wheat grain yield by manipulating the AGL6 gene.

SUBMITTER: Kong X

PROVIDER: S-EPMC8710900 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: The MADS-box transcription factors play fundamental roles in reproductive developmental control. Although the roles of many plant MADS-box proteins have been extensively studied, there are almost no functional studies of them in soybean, an important protein and oil crop in the world. In addition, the MADS-box protein orthologs may have species-specific functions. Controlling male fertility is an important goal in plant hybrid breeding but is difficult in some crops like soybean. The morphological structure of soybean flowers prevents the cross-pollination. Understanding the molecular mechanisms for floral development will aid in engineering new sterile materials that could be applied in hybrid breeding programs in soybean. RESULT: Through microarray analysis, a flower-enriched gene in soybean was selected and designated as GmMADS28. GmMADS28 belongs to AGL9/SEP subfamily of MADS-box proteins, localized in nucleus and showed specific expression patterns in floral meristems as well as stamen and petal primordia. Expression of GmMADS28 in the stamens and petals of a soybean mutant NJS-10Hfs whose stamens are converted into petals was higher than in those of wild-type plants. Constitutive expression of GmMADS28 in tobacco promoted early flowering and converted stamens and sepals to petals. Interestingly, transgenic plants increased the numbers of sepal, petal and stamen from five to six and exhibited male sterility due to the shortened and curly filaments and the failure of pollen release from the anthers. The ectopic expression of GmMADS28 was found to be sufficient to activate expression of tobacco homologs of SOC1, LEAFY, AGL8/FUL, and DEF. In addition, we observed the interactions of GmMADS28 with soybean homologs of SOC1, AP1, and AGL8/FUL proteins. CONCLUSION: In this study, we observed the roles of GmMADS28 in the regulation of floral organ number and petal identity. Compared to other plant AGL9/SEP proteins, GmMADS28 specifically regulates floral organ number, filament length and pollen release. The sterility caused by the ectopic expression of GmMADS28 offers a promising way to genetically produce new sterile material that could potentially be applied in the hybrid breeding of crops like soybean.

Project description:BackgroundThe morphological diversity of flower organs is closely related to functional divergence within the MADS-box gene family. Bryophytes and seedless vascular plants have MADS-box genes but do not have ABCDE or AGAMOUS-LIKE6 (AGL6) genes. ABCDE and AGL6 genes belong to the subgroup of MADS-box genes. Previous works suggest that the B gene was the first ABCDE and AGL6 genes to emerge in plant but there are no mentions about the probable origin time of ACDE and AGL6 genes. Here, we collected ABCDE and AGL6 gene 381 protein sequences and 361 coding sequences from gymnosperms and angiosperms and reconstructed a complete Bayesian phylogeny of these genes. In this study, we want to clarify the probable origin time of ABCDE and AGL6 genes is a great help for understanding the role of the formation of the flower, which can decipher the forming order of MADS-box genes in the future.ResultsThese genes appeared to have been under purifying selection and their evolutionary rates are not significantly different from each other. Using the Bayesian evolutionary analysis by sampling trees (BEAST) tool, we estimated that: the mutation rate of the ABCDE and AGL6 genes was 2.617 × 10-3 substitutions/site/million years, and that B genes originated 339 million years ago (MYA), CD genes originated 322 MYA, and A genes shared the most recent common ancestor with E/AGL6 296 MYA, respectively.ConclusionsThe phylogeny of ABCDE and AGL6 genes subfamilies differed. The APETALA1 (AP1 or A gene) subfamily clustered into one group. The APETALA3/PISTILLATA (AP3/PI or B genes) subfamily clustered into two groups: the AP3 and PI clades. The AGAMOUS/SHATTERPROOF/SEEDSTICK (AG/SHP/STK or CD genes) subfamily clustered into a single group. The SEPALLATA (SEP or E gene) subfamily in angiosperms clustered into two groups: the SEP1/2/4 and SEP3 clades. The AGL6 subfamily clustered into a single group. Moreover, ABCDE and AGL6 genes appeared in the following order: AP3/PI → AG/SHP/STK → AGL6/SEP/AP1. In this study, we collected candidate sequences from gymnosperms and angiosperms. This study highlights important events in the evolutionary history of the ABCDE and AGL6 gene families and clarifies their evolutionary path.

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The wheat AGL6-like MADS-box gene is a master regulator for floral organ identity and a target for spikelet meristem development manipulation.

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