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Evolution and Diversification of FRUITFULL Genes in Solanaceae.

ABSTRACT: Ecologically and economically important fleshy edible fruits have evolved from dry fruit numerous times during angiosperm diversification. However, the molecular mechanisms that underlie these shifts are unknown. In the Solanaceae there has been a major shift to fleshy fruits in the subfamily Solanoideae. Evidence suggests that an ortholog of FRUITFULL (FUL), a transcription factor that regulates cell proliferation and limits the dehiscence zone in the silique of Arabidopsis, plays a similar role in dry-fruited Solanaceae. However, studies have shown that FUL orthologs have taken on new functions in fleshy fruit development, including regulating elements of tomato ripening such as pigment accumulation. FUL belongs to the core eudicot euFUL clade of the angiosperm AP1/FUL gene lineage. The euFUL genes fall into two paralogous clades, euFULI and euFULII. While most core eudicots have one gene in each clade, Solanaceae have two: FUL1 and FUL2 in the former, and MBP10 and MBP20 in the latter. We characterized the evolution of the euFUL genes to identify changes that might be correlated with the origin of fleshy fruit in Solanaceae. Our analyses revealed that the Solanaceae FUL1 and FUL2 clades probably originated through an early whole genome multiplication event. By contrast, the data suggest that the MBP10 and MBP20 clades are the result of a later tandem duplication event. MBP10 is expressed at weak to moderate levels, and its atypical short first intron lacks putative transcription factor binding sites, indicating possible pseudogenization. Consistent with this, our analyses show that MBP10 is evolving at a faster rate compared to MBP20. Our analyses found that Solanaceae euFUL gene duplications, evolutionary rates, and changes in protein residues and expression patterns are not correlated with the shift in fruit type. This suggests deeper analyses are needed to identify the mechanism underlying the change in FUL ortholog function.

SUBMITTER: Maheepala DC

PROVIDER: S-EPMC6394111 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Evolution and Diversification of FRUITFULL Genes in Solanaceae.

Maheepala Dinusha C DC Emerling Christopher A CA Rajewski Alex A Macon Jenna J Strahl Maya M Pabón-Mora Natalia N Litt Amy A

Frontiers in plant science 20190221

Ecologically and economically important fleshy edible fruits have evolved from dry fruit numerous times during angiosperm diversification. However, the molecular mechanisms that underlie these shifts are unknown. In the Solanaceae there has been a major shift to fleshy fruits in the subfamily Solanoideae. Evidence suggests that an ortholog of FRUITFULL (FUL), a transcription factor that regulates cell proliferation and limits the dehiscence zone in the silique of Arabidopsis ...[more]

PMID: 30846991

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Project description:Background and Aims:The genetic basis of fruit development has been extensively studied in Arabidopsis, where major transcription factors controlling valve identity (i.e. FRUITFULL), replum development (i.e. REPLUMLESS) and the differentiation of the dehiscence zones (i.e. SHATTERPROOF, INDEHISCENT and ALCATRAZ) have been identified. This gene regulatory network in other flowering plants is influenced by duplication events during angiosperm diversification. Here we aim to characterize candidate fruit development genes in the Solanaceae and compare them with those of Brassicaceae. Methods:ALC/SPT, HEC/IND, RPL and AG/SHP homologues were isolated from publicly available databases and from our own transcriptomes of Brunfelsia australis and Streptosolen jamesonii. Maximum likelihood phylogenetic analyses were performed for each of the gene lineages. Shifts in protein motifs, as well as expression patterns of all identified homologues, are shown in dissected floral organs and fruits in different developmental stages of four Solanaceae species exhibiting different fruit types. Key Results:Each gene lineage has undergone different duplication time-points, resulting in very different genetic complements in the Solanaceae when compared with the Brassicaceae. In general, Solanaceae species have more copies of HEC1/2 and RPL than Brassicaceae, have fewer copies of SHP and the same number of copies of AG, ALC and SPT. Solanaceae lack IND orthologues, but have pre-duplication HEC3 homologues. The expression analyses showed opposite expression of SPT and ALC orthologues between dry- and fleshy-fruited species during fruit maturation. Fleshy-fruited species turn off RPL and SPT orthologues during maturation. Conclusions:The gynoecium patterning and fruit developmental genetic network in the Brassicaceae cannot be directly extrapolated to the Solanaceae. In Solanaceae ALC, SPT and RPL contribute differently to maturation of dry dehiscent and fleshy fruits, whereas HEC genes are not generally expressed in the gynoecium. RPL genes have broader expression patterns than expected.

Project description:Background and aimsCapsicum (Solanaceae), native to the tropical and temperate Americas, comprises the well-known sweet and hot chili peppers and several wild species. So far, only partial taxonomic and phylogenetic analyses have been done for the genus. Here, the phylogenetic relationships between nearly all taxa of Capsicum were explored to test the monophyly of the genus and to obtain a better knowledge of species relationships, diversification and expansion.MethodsThirty-four of approximately 35 Capsicum species were sampled. Maximum parsimony and Bayesian inference analyses were performed using two plastid markers (matK and psbA-trnH) and one single-copy nuclear gene (waxy). The evolutionary changes of nine key features were reconstructed following the parsimony ancestral states method. Ancestral areas were reconstructed through a Bayesian Markov chain Monte Carlo analysis.Key resultsCapsicum forms a monophyletic clade, with Lycianthes as a sister group, following both phylogenetic approaches. Eleven well-supported clades (four of them monotypic) can be recognized within Capsicum, although some interspecific relationships need further analysis. A few features are useful to characterize different clades (e.g. fruit anatomy, chromosome base number), whereas some others are highly homoplastic (e.g. seed colour). The origin of Capsicum is postulated in an area along the Andes of western to north-western South America. The expansion of the genus has followed a clockwise direction around the Amazon basin, towards central and south-eastern Brazil, then back to western South America, and finally northwards to Central America.ConclusionsNew insights are provided regarding interspecific relationships, character evolution, and geographical origin and expansion of Capsicum A clearly distinct early-diverging clade can be distinguished, centred in western-north-western South America. Subsequent rapid speciation has led to the origin of the remaining clades. The diversification of Capsicum has culminated in the origin of the main cultivated species in several regions of South to Central America.

Project description:Myeloblastosis (MYB) genes are important transcriptional regulators of plant growth, development, and secondary metabolic biosynthesis pathways, such as capsaicinoid biosynthesis in Capsicum. Although MYB genes have been identified in Capsicum annuum, no comprehensive study has been conducted on other Capsicum species. We identified a total of 251 and 240 MYB encoding genes in Capsicum chinense MYBs (CcMYBs) and Capsicum baccatum MYBs (CbMYBs). The observation of twenty tandem and 41 segmental duplication events indicated expansion of the MYB gene family in the C. chinense genome. Five CcMYB genes, i.e., CcMYB101, CcMYB46, CcMYB6, CcPHR8, and CcRVE5, and two CaMYBs, i.e., CaMYB3 and CaHHO1, were found within the previously reported capsaicinoid biosynthesis quantitative trait loci. Based on phylogenetic analysis with tomato MYB proteins, the Capsicum MYBs were classified into 24 subgroups supported by conserved amino acid motifs and gene structures. Also, a total of 241 CcMYBs were homologous with 225 C. annuum, 213 C. baccatum, 125 potato, 79 tomato, and 23 Arabidopsis MYBs. Synteny analysis showed that all 251 CcMYBs were collinear with C. annuum, C. baccatum, tomato, potato, and Arabidopsis MYBs spanning over 717 conserved syntenic segments. Using transcriptome data from three fruit developmental stages, a total of 54 CcMYBs and 81 CaMYBs showed significant differential expression patterns. Furthermore, the expression of 24 CcMYBs from the transcriptome data was validated by quantitative real-time (qRT) PCR analysis. Eight out of the 24 CcMYBs validated by the qRT-PCR were highly expressed in fiery hot C. chinense than in the lowly pungent C. annuum. Furthermore, the co-expression analysis revealed several MYB genes clustered with genes from the capsaicinoid, anthocyanin, phenylpropanoid, carotenoid, and flavonoids biosynthesis pathways, and related to determining fruit shape and size. The homology modeling of 126 R2R3 CcMYBs showed high similarity with that of the Arabidopsis R2R3 MYB domain template, suggesting their potential functional similarity at the proteome level. Furthermore, we have identified simple sequence repeat (SSR) motifs in the CcMYB genes, which could be used in Capsicum breeding programs. The functional roles of the identified CcMYBs could be studied further so that they can be manipulated for Capsicum trait improvement.

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Project description:BackgroundCatalases (CATs) break down hydrogen peroxide into water and oxygen to prevent cellular oxidative damage, and play key roles in the development, biotic and abiotic stresses of plants. However, the evolutionary relationships of the plant CAT gene family have not been systematically reported.ResultsHere, we conducted genome-wide comparative, phylogenetic, and structural analyses of CAT orthologs from 29 out of 31 representative green lineage species to characterize the evolution and functional diversity of CATs. We found that CAT genes in land plants were derived from core chlorophytes and detected a lineage-specific loss of CAT genes in Fabaceae, suggesting that the CAT genes in this group possess divergent functions. All CAT genes were split into three major groups (group α, β1, and β2) based on the phylogeny. CAT genes were transferred from bacteria to core chlorophytes and charophytes by lateral gene transfer, and this led to the independent evolution of two types of CAT genes: α and β types. Ten common motifs were detected in both α and β groups, and β CAT genes had five unique motifs, respectively. The findings of our study are inconsistent with two previous hypotheses proposing that (i) new CAT genes are acquired through intron loss and that (ii) the Cys-343 residue is highly conserved in plants. We found that new CAT genes in most higher plants were produced through intron acquisition and that the Cys-343 residue was only present in monocots, Brassicaceae and Pp_CatX7 in P. patens, which indicates the functional specificity of the CATs in these three lineages. Finally, our finding that CAT genes show high overall sequence identity but that individual CAT genes showed developmental stage and organ-specific expression patterns suggests that CAT genes have functionally diverged independently.ConclusionsOverall, our analyses of the CAT gene family provide new insights into their evolution and functional diversification in green lineage species.

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Evolution and Diversification of FRUITFULL Genes in Solanaceae.

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Evolution and Diversification of <i>FRUITFULL</i> Genes in Solanaceae.

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