Mutations in the SmAPRR2 transcription factor suppressing chlorophyll pigmentation in the eggplant fruit peel are key drivers of a diversified colour palette

Abstract

Understanding the mechanisms by which chlorophylls are synthesized in the eggplant (Solanum melongena) fruit peel is of great relevance for eggplant breeding. A multi-parent advanced generation inter-cross (MAGIC) population and a germplasm collection have been screened for green pigmentation in the fruit peel and used to identify candidate genes for this trait. A genome-wide association study (GWAS) performed with 420 MAGIC individuals revealed a major association on chromosome 8 close to a gene similar to APRR2. Two variants in SmAPRR2, predicted as having a high impact effect, were associated with the absence of fruit chlorophyll pigmentation in the MAGIC population, and a large deletion of 5.27 kb was found in two reference genomes of accessions without chlorophyll in the fruit peel. The validation of the candidate gene SmAPRR2 was performed by its sequencing in a set of MAGIC individuals and through its de novo assembly in 277 accessions from the G2P-SOL eggplant core collection. Two additional mutations in SmAPRR2 associated with the lack of chlorophyll were identified in the core collection set. The phylogenetic analysis of APRR2 reveals orthology within Solanaceae and suggests that specialization of APRR2-like genes occurred independently in Cucurbitaceae and Solanaceae. A strong geographical differentiation was observed in the frequency of predominant mutations in SmAPRR2, resulting in a lack of fruit chlorophyll pigmentation and suggesting that this phenotype may have arisen and been selected independently several times. This study represents the first identification of a major gene for fruit chlorophyll pigmentation in the eggplant fruit.

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

“…The GLKs transcription factors (TFs) belong to a GARP superfamily TF whose functions are important for the expression of nuclear photosynthesis-related genes and for chloroplast development in both leaves and fruits ( Riechmann et al., 2000 ; Hosoda et al., 2002 ; Waters et al., 2008 ; Nguyen et al., 2014 ). The APRR2 orthologs have been shown to regulate chlorophyll content in a wide range of crops from Solanaceae and Cucurbitaceae including tomato, pepper, eggplants, cucumber, melon, watermelon, wax gourd, and Zucchini ( Pan et al., 2013 ; Liu et al., 2016 ; Oren et al., 2019 ; Jeong et al., 2020 ; Ma et al., 2021 ; Arrones et al., 2022 ; Zhu et al., 2022 ; Fang et al., 2023 ). These genes are found to associate with increased plastid numbers and chlorophyll accumulation of fruit colors in immature fruit peels, resulted in white or light green.…”

Multi‐environment association study highlights candidate genes for robust agronomic quantitative trait loci in a novel worldwide Capsicum core collection

“…A homolog of the probable leucine-rich repeat receptor-like protein kinase of the Candidate genes for fruit color Among the 16 candidate genes for immature fruit color, we highlighted two strong candidate genes for four QTLs. Homologs of transcription factor ARABIDOPSIS PSEUDO RESPONSE REGULATOR2 (APRR2) determine mature or immature fruit color in numerous cucurbits and solanaceous crops including melon (Oren et al, 2019), watermelon (Oren et al, 2019), cucumber (Liu et al, 2016;Tang et al, 2018), zucchini (Montero-Pau et al, 2017, wax gourd (Ma et al, 2021), tomato (Pan et al, 2013), eggplant (Arrones et al, 2022;Fang et al, 2023), as well as stem color in squash (Zhu et al, 2022). The pepper homolog of APRR2 on chromosome P1 corresponds to the well-known mature fruit color locus c1 (Kormos & Kormos, 1960), which was also shown to regulate chlorophyll content and immature fruit color (Jeong et al, 2020;Lee, Kim, et al, 2020;Pan et al, 2013) via regulating thylakoid numbers and chloroplast size (Lee, Kim, et al, 2020).…”

The irregular fruit green netting: An eggplant domestication trait controlled by theSmGLK2gene with implications in fruit colour diversification

“…A total of 420 individuals from the eggplant S3MEGGIC population developed by Mangino et al (2022) were used to identify candidate genomic regions associated with the FN trait. This population was previously used for identifying SmAPRR2 as the causative gene for uniform chlorophyll pigmentation in the eggplant fruit peel (Arrones et al, 2022). The S3MEGGIC population was obtained by inter-crossing seven Solanum melongena accession and one wild S. incanum INC accession (Figure 1A).…”

“…Variation in the presence or absence of chlorophylls in the eggplant (Solanum melongena L.) fruit peel contributes to the wide range of fruit colours in this species (Arrones et al, 2022). Furthermore, the distribution of chlorophylls can be uniform or irregular, the latter being referred to as netting, reticulation, or variegation (Tigchelaar, 1968;Daunay et al, 2004).…”