Transcriptome Profiling of Tomato Uncovers an Involvement of Cytochrome P450s and Peroxidases in Stigma Color Formation

Abstract

Stigma is a crucial structure of female reproductive organ in plants. Stigma color is usually regarded as an important trait in variety identification in some species, but the molecular mechanism of stigma color formation remains elusive. Here, we characterized a tomato mutant, yellow stigma (ys), that shows yellow rather than typical green color in the stigma. Analysis of pigment contents revealed that the level of flavonoid naringenin chalcone was increased in the ys stigma, possibly as a result of higher accumulation of p-coumaric acid, suggesting that naringenin chalcone might play a vital role in yellow color control in tomato stigma. To understand the genes and gene networks that regulate tomato stigma color, RNA-sequencing (RNA-Seq) analyses were performed to compare the transcriptomes of stigmas between ys mutant and wild-type (WT). We obtained 507 differentially expressed genes, in which, 84 and 423 genes were significantly up-regulated and down-regulated in the ys mutant, respectively. Two cytochrome P450 genes, SlC3H1 and SlC3H2 which encode p-coumarate 3-hydroxylases, and six peroxidase genes were identified to be dramatically inhibited in the yellow stigma. Further bioinformatic and biochemical analyses implied that the repression of the two SlC3Hs and six PODs may indirectly lead to higher naringenin chalcone level through inhibiting lignin biosynthesis, thereby contributing to yellow coloration in tomato stigma. Thus, our data suggest that two SlC3Hs and six PODs are involved in yellow stigma formation. This study provides valuable information for dissecting the molecular mechanism of stigma color control in tomato.Statement: This study reveals that two cytochrome P450s (SlC3H1 and SlC3H2) and six peroxidases potentially regulate the yellow stigma formation by indirectly enhancing biosynthesis of yellow-colored naringenin chalcone in the stigma of tomato.

Map-based cloning of the APRR2 gene controlling green stigma in bitter gourd (Momordica charantia)

“…In a rice indica cultivar, its purple apiculi and stigma were genetic regulated by the interaction of two genes involved the anthocyanin biosynthesis pathway: OsC1 (encoding a R2R3-MYB transcription factor) and OsDFR (encoding a dihyroflavonol 4-reductase) ( Meng et al., 2021 ). Recent two transcriptomic studies aimed at revealing the gene network were conducted and showed that the yellow stigma in tomato is very likely due to the accumulation of yellow-colored flavonoid naringenin chalcone, whereas the melon yellow stigma is due to break-down of chloroplast structure interfering chlorophyll biosynthesis ( Zhang et al., 2017 ; Lv et al., 2022a ). Despite the crucial functional roles of stigmas play in plant reproduction, there has not been sufficient researches dedicated to the color of stigma.…”

Expanding Alternative Splicing Identification by Integrating Multiple Sources of Transcription Data in Tomato

“…A number of well-designed experiments in genome-wide transcriptome analysis for identifying differentially expressed genes and/or AS in tomato, a model plant specifically for fruit development, have been reported in recent few years. These studies include comparative transcriptome analysis of domesticated tomato for identifying differentially expressed genes in different tissues (Lopez-Casado et al, 2012; Koenig et al, 2013; Zouine et al, 2014; Sun and Xiao, 2015; Sundaresan et al, 2016; Wang K. et al, 2016; Zhang Y. et al, 2017), diurnal transcriptome changes (Higashi et al, 2016), global transcriptome profiles of tomato leaf responses to exogenous ABA or cytokinin (Wang et al, 2013; Shi et al, 2013), root transcriptome regulations in response to different plant hormone cytokinin and auxin (Gupta et al, 2013), transcriptome profiles with a focus on fruit development or in different fruit tissues (Ye et al, 2015; Zhang S. et al, 2016; Dai et al, 2017; Ezura et al, 2017) and fruit chilling tolerance (Cruz-Mendívil et al, 2015). RNA-seq data were also collected for analysis of differential gene expressions in response to tomato yellow leaf curl virus (TYLCV) infection in the TYLCV-resistant (R) breeding line and TYLCV-susceptible breeding line (Chen et al, 2013), in response to tobacco rattle virus (TRV) (Zheng et al, 2017), Pseudomonas syringae (Yang et al, 2015; Worley et al, 2016), Xanthomonas perforans (Du et al, 2015), Cladosporium fulvum (Xue et al, 2016), Colletotrichum gloeosporioides (Alkan et al, 2015), Verticillium dahlia (Tan et al, 2015), Meloidogyne incognita (root-knot nematode) (Shukla et al, 2018) and in arbuscular mycorrhiza inoculated and control plants (Zouari et al, 2014).…”

Comparative transcriptome analysis provides global insight into gene expression differences between two orchid cultivars

“…In plants, P450s are involved in metabolism processes related to pigment formation, defence response, photosynthesis, respiration, etc [ 37 ]. In tomato, Zhang et al [ 38 ] found that two cytochrome P450s regulate yellow stigma formation by indirectly enhancing the biosynthesis of yellow-coloured naringenin chalcone in the stigma of tomato. Fatty acid metabolism not only produces energy but also provides a carbon skeleton for organic compound formation.…”