Giberellic Acid-Stimulated Transcript Proteins Evolved through Successive Conjugation of Novel Motifs and Their Subfunctionalization

Abstract

Gibberellic Acid Stimulated Transcript (GAST)-like genes encode small polypeptides, some of which have been implicated in diverse biological processes regulating plant growth and development. However, the occurrence of GASTs among plants, their protein structures, and the mechanisms by which they evolved remain elusive. Here, using a customized workflow, we report genes encoding GAST proteins, identify novel motifs and evolutionary patterns contributing to the subfunctionalization of GAST domains, and explore functional conservation across diverse plant groups. We show that GAST-like sequences evolved initially in the vascular plant Selaginella moellendorffii, after the divergence from bryophytes, and later emerged in gymnosperms and angiosperms. GASTs in angiosperms are characterized by four conserved novel motifs; however, relatively fewer conserved motifs exist in pteridophytes and gymnosperms. Phylogenetic analysis revealed that the GAST-Cysteine Rich1 motif evolved early in the S. moellendorffii GAST, which further acquired subfunctionalization through successive conjugation of other motifs and remained conserved across plants, as supported by their collinearity. Functional characterization of two orthologs from the dicot Arabidopsis (Arabidopsis thaliana; Gibberellic Acid-Stimulated Arabidopsis 10) and the monocot rice (Oryza sativa; Gibberellic Acid Stimulated Transcript-Related 9) suggests hormonal regulation, novel roles in seed germination, and functional conservation among diverse plant groups. Computational modeling predicts that these GAST genes are regulated by several factors, including the phytohormones gibberellin and abscisic acid, through conserved cis-motifs present in their promoters, and that they might act as signaling molecules in a complex feedback loop. Thus, our study identifies GASTs and their encoded proteins, uncovers their structure, novel motifs, and evolutionary pattern among plants, and suggests their functional conservation.

GhGASA10-1 promotes the cell and fiber elongation through the phytohormones IAA-induced

“…The GASA proteins are quite conservative in higher plants, mainly divided into three subgroups in Arabidopsis and Gossypium, which is consistent with GASA family of Zea mays [10], Oryza sativa [11,21], Vitis vinifera [12], and Glycine max [17]. GASA genes are present in lower fern plants S. moellendor i [11]. In the life tree, the number of GASA genes have hardly changed from ferns to angiosperms, rstly reported in our study.…”

“…This differential distribution of GASA family genes emphasized the loss of genes in different allotetraploid cotton species, consistent with the higher rate of gene loss in different allotetraploid cotton than in diploid species [15,40]. The GASA proteins are quite conservative in higher plants, mainly divided into three subgroups in Arabidopsis and Gossypium, which is consistent with GASA family of Zea mays [10], Oryza sativa [11,21], Vitis vinifera [12], and Glycine max [17]. GASA genes are present in lower fern plants S. moellendor i [11].…”

“…Gibberellic Acid Stimulated Transcript (GAST)-like genes have been involved in complicated biological processes modifying further plant growth and development [11]. In most of the plants, GASAs domains are greatly conserved, resulting in conserved proteins [10,12].…”

“…The presence conserved motifs is the main reason for GASTs to be conserved in vascular plants. Further, the phylogenetic studies of GASTs family genes from plant kingdom showed that GASTs might be initially evolved in S. moellendor i [11]. GAST1, which is one of GAST family genes, initially detected in tomato [16] with subsequent discoveries in different species, such maize (Zea mays L.) [10], Arabidopsis [11], Glycine max [17], Grapevine (Vitis vinifera L.) [12].…”

“…Interestingly, two vertical homologies from Arabidopsis (AtGASA10) and rice (OsGAST9) showed conserved (Functional and structural) positive regulatory role in germination, between dicot and monocot plants. Phytohormones may regulate both AtGASA10 and OsGASR9 through the signal element in their promoter reigons and correspond to the signal element in likely feedback/responce cycles in GA/ABAmediated regulation [11]. GAs are among the universal plant phytoharmones that play crucial role in the growth and development processes including germination, stem elongation, photosynthesis, owering, and seed development, while GASA-like genes possess a key role in GAs signaling pathway [12,22,23] in different plants viz.…”