Intraspecific divergence study of TCP (teosinte branched [TB1], cycloidea [CYC] and proliferating cell factors [PCF]) transcription factors was conducted in Indian and Chinese varieties including landraces of sesame to understand the effects of breeding and adaptive selection on genomic architecture. The varieties included “Swetha,” a pedigree selection and “Zhongzhi‐13,” a space mutant; whereas the landraces studied were “Baizhima” and “Mishouzhima” adapted to widely different ecological niches. “Swetha” the Indian variety contained 33 TCP genes, including 14 Class‐I and 19 Class‐II genes, whereas “Zhongzhi‐13” the RefSeq variety contained 13 Class‐I and 15 Class‐II genes. Sixteen Class‐I genes and six CYC genes were common in both the landraces whereas an additional gene variant was found in “Baizhima.” Class‐II TCP genes were found more conserved within species while Class‐I genes differed widely within and across species. A cluster of 12 Class‐I genes was found unique to the Chinese genotypes, whereas two of the Class‐I genes in landrace “Baizhima” were found more similar to the Indian variety “Swetha” genes. A varied number of retrocopies and retropseudogenes were also found among Class‐I TCPs, due to insertion of TY1/Copia transposons. A number of active TY1/Copia retrotransposons containing “chimeric retrogenes” with multiple introns were discovered in sesame. One set involved “SiwTCP3” from “Swetha” and its homologues from the landraces with a mutation in the conserved Cys‐20 residue which abolished the redox sensitivity whereas the second set was present only in the landraces without the above mutation. None of the “Zhongzhi‐13” genes contained TY1/Copia insertions. Transposon insertions resulted in heavy methylation of unique genes in “Swetha” while methylation spread was noticed in the upstream and downstream regulatory regions. Although CIN‐TCPs were established as preferred binding partners of phytoplasma effectors, we found many mutations in the functional domains which altered the protein folding mechanisms among the protein homologues, with one set reported unique in the Chinese varieties. More duplication was noted in the CIN‐TCP's of “Swetha” whereas multiple exons and exon fusions resulted in the acquisition of novel functions for sesame TCP genes. The insertions, deletions and the duplications acquired through genome evolution under marginal environment conditions altered the binding abilities of CIN‐TCP transcription factors which ultimately resulted in variable response to sesame phyllody caused by phytoplasma.
Evolutionary dynamics of AP2/ERF and WRKY genes, the major components of defense response were studied extensively in the sesame pan-genome. Massive variation was observed for gene copy numbers, genome location, domain structure, exon-intron structure and protein parameters. In the pan-genome, 63% of AP2/ERF members were devoid of introns whereas >99% of WRKY genes contained multiple introns. AP2 subfamily was found to be micro-exon rich with the adjoining intronic sequences sharing sequence similarity to many stress-responsive and fatty acid metabolism genes. WRKY family included extensive multi-domain gene fusions where the additional domains significantly enhanced gene and exonic sizes as well as gene copy numbers. The fusion genes were found to have roles in acquired immunity, stress response, cell and membrane integrity as well as ROS signaling. The individual genomes shared extensive synteny and collinearity although ecological adaptation was evident among the Chinese and Indian accessions. Significant positive selection effects were noticed for both micro-exon and multi-domain genes. Splice variants with changes in acceptor, donor and branch sites were common and 6-7 splice variants were detected per gene. The study ascertained vital roles of lipid metabolism and chlorophyll biosynthesis in the defense response and stress signaling pathways. 60% of the studied genes localized in the nucleus while 20% preferred chloroplast. Unique cis-element distribution was noticed in the upstream promoter region with MYB and STRE in WRKY genes while MYC was present in the AP2/ERF genes. Intron-less genes exhibited great diversity in the promoter sequences wherein the predominance of dosage effect indicated variable gene expression levels. Mimicking the NBS-LRR genes, a chloroplast localized WRKY gene, Swetha_24868, with additional domains of chorismate mutase, cAMP and voltage-dependent potassium channel was found to act as a master regulator of defense signaling, triggering immunity and reducing ROS levels.
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