Color and pigment contents are important aspects of fruit quality and consumer acceptance of cucurbit crops. Here, we describe the independent mapping and cloning of a common causative APRR2 gene regulating pigment accumulation in melon and watermelon. We initially show that the APRR2 transcription factor is causative for the qualitative difference between dark and light green rind in both crops. Further analyses establish the link between sequence or expression level variations in the CmAPRR2 gene and pigment content in the rind and flesh of mature melon fruits. A genome-wide association study (GWAS) of young fruit rind color in a panel composed of 177 diverse melon accessions did not result in any significant association, leading to an earlier assumption that multiple genes are involved in shaping the overall phenotypic variation in this trait. Through resequencing of 25 representative accessions and allelism tests between light rind accessions, we show that multiple independent single nucleotide polymorphisms in the CmAPRR2 gene are causative of the light rind phenotype. The multi-haplotypic nature of this gene explains the lack of detection power obtained through genotyping by sequencing-based GWAS and confirms the pivotal role of this gene in shaping fruit color variation in melon. This study demonstrates the power of combining bi- and multi-allelic designs with deep sequencing, to resolve lack of power due to high haplotypic diversity and low allele frequencies. Due to its central role and broad effect on pigment accumulation in fruits, the APRR2 gene is an attractive target for carotenoid bio-fortification of cucurbit crops.
SUMMARYIn the development of tomato compound leaves, local auxin maxima points, separated by the expression of the Aux/IAA protein SlIAA9/ENTIRE (E), direct the formation of discrete leaflets along the leaf margin. The local auxin maxima promote leaflet initiation, while E acts between leaflets to inhibit auxin response and lamina growth, enabling leaflet separation. Here, we show that a group of auxin response factors (ARFs), which are targeted by miR160, antagonizes auxin response and lamina growth in conjunction with E. In wild-type leaf primordia, the miR160-targeted ARFs SlARF10A and SlARF17 are expressed in leaflets, and SlmiR160 is expressed in provascular tissues. Leaf overexpression of the miR160-targeted ARFs SlARF10A, SlARF10B or SlARF17, led to reduced lamina and increased leaf complexity, and suppressed auxin response in young leaves. In agreement, leaf overexpression of miR160 resulted in simplified leaves due to ectopic lamina growth between leaflets, reminiscent of e leaves. Genetic interactions suggest that E and miR160-targeted ARFs act partially redundantly but are both required for local inhibition of lamina growth between initiating leaflets. These results show that different types of auxin signal antagonists act cooperatively to ensure leaflet separation in tomato leaf margins.
23Color and pigment content are important aspects of fruit quality and consumer 24 acceptance of cucurbit crops. Here, we describe the independent mapping and cloning 25 of a common causative APRR2 gene regulating pigment accumulation in melon and 26 watermelon. We initially show that the APRR2 transcription factor is causative for the 27 qualitative difference between dark and light green rind in both crops. Further analyses 28 establish the link between sequence or expression level variations in the CmAPRR2 29 gene and pigments content in the rind and flesh of mature melon fruits. GWAS of young 30 fruit rind color in a panel composed of 177 diverse melon accessions did not result in 31 any significant association, leading to an earlier assumption that multiple genes are 32 involved in shaping the overall phenotypic variation at this trait. Through resequencing 33 of 25 representative accessions and allelism tests between light rind accessions, we 34 show that multiple independent SNPs in the CmAPRR2 gene are causative for the light 35 rind phenotype. The multi-haplotypic nature of this gene explain the lack of detection 36 power obtained through GBS-based GWAS and confirm the pivotal role of this gene in 37 shaping fruit color variation in melon. This study demonstrates the power of combining 38 bi-and multi-allelic designs with deep sequencing, to resolve lack of power due to high 39 haplotypic diversity and low allele frequencies. Due to its central role and broad effect 40 on pigment accumulation in fruits, the APRR2 gene is an attractive target for 41 carotenoids bio-fortification of cucurbit crops.42 43
Earliness and ripening behavior are important attributes of fruits on and off the vine, and affect quality and preference of both growers and consumers. Fruit ripening is a complex physiological process that involves metabolic shifts affecting fruit color, firmness, and aroma production. Melon is a promising model crop for the study of fruit ripening, as the full spectrum of climacteric behavior is represented across the natural variation. Using Recombinant Inbred Lines (RILs) population derived from the parental lines “Dulce” (reticulatus, climacteric) and “Tam Dew” (inodorus, non-climacteric) that vary in earliness and ripening traits, we mapped QTLs for ethylene emission, fruit firmness and days to flowering and maturity. To further annotate the main QTL intervals and identify candidate genes, we used Oxford Nanopore long-read sequencing in combination with Illumina short-read resequencing, to assemble the parental genomes de-novo. In addition to 2.5 million genome-wide SNPs and short InDels detected between the parents, we also highlight here the structural variation between these lines and the reference melon genome. Through systematic multi-layered prioritization process, we identified 18 potential polymorphisms in candidate genes within multi-trait QTLs. The associations of selected SNPs with earliness and ripening traits were further validated across a panel of 177 diverse melon accessions and across a diallel population of 190 F1 hybrids derived from a core subset of 20 diverse parents. The combination of advanced genomic tools with diverse germplasm and targeted mapping populations is demonstrated as a way to leverage forward genetics strategies to dissect complex horticulturally important traits.
Heterosis, the superiority of hybrids over their parents, is a major genetic force associated with plant fitness and crop yield enhancement. Understanding and predicting heterosis is crucial for evolutionary biology, as well as for plant and animal breeding. We investigated root-mediated yield heterosis in melons (Cucumis melo) by characterizing common variety grafted onto 190 hybrid rootstocks resulting from crossing 20 diverse inbreds in a diallel-mating scheme. Hybrid rootstocks improved yield by more than 40% compared to their parents and the best hybrid outperformed the reference commercial variety by 65% under both optimal and minimal irrigation treatments. To characterize the genetics of the underground heterosis we conducted whole-genome re-sequencing of the 20 founder lines, and showed that parental genetic distance was no predictor for the level of heterosis. Through inference of the 190 hybrids genotypes from their parental genomes, followed by genome-wide association analysis, we mapped multiple root-mediated yield QTLs. The yield enhancement of the four best-performing hybrid rootstocks was validated in multiple experiments with four different scion varieties. While root biology is receiving increased attention, most of the research is conducted using plants not amenable to grafting and, as a result, it is difficult to separate root and shoot effects. Here, we use the rich genetic and genomic resources of Cucumis melo, where grafting is a common practice, to dissect a unique phenomenon of root-mediated yield heterosis, by directly evaluating in the field the contribution of the roots to fruit yield. Our grafting approach is complementary to the common roots genetics research path that focuses mainly on variation in root system architecture rather than the ultimate root-mediated whole-plant performance, and is a step towards discovery of candidate genes involved in root function and yield enhancement.
SUMMARY Linking genotype with phenotype is a fundamental goal in biology and requires robust data for both. Recent advances in plant‐genome sequencing have expedited comparisons among multiple‐related individuals. The abundance of structural genomic within‐species variation that has been discovered indicates that a single reference genome cannot represent the complete sequence diversity of a species, leading to the expansion of the pan‐genome concept. For high‐resolution forward genetics, this unprecedented access to genomic variation should be paralleled and integrated with phenotypic characterization of genetic diversity. We developed a multi‐parental framework for trait dissection in melon (Cucumis melo), leveraging a novel pan‐genome constructed for this highly variable cucurbit crop. A core subset of 25 diverse founders (MelonCore25), consisting of 24 accessions from the two widely cultivated subspecies of C. melo, encompassing 12 horticultural groups, and 1 feral accession was sequenced using a combination of short‐ and long‐read technologies, and their genomes were assembled de novo. The construction of this melon pan‐genome exposed substantial variation in genome size and structure, including detection of ~300 000 structural variants and ~9 million SNPs. A half‐diallel derived set of 300 F2 populations, representing all possible MelonCore25 parental combinations, was constructed as a framework for trait dissection through integration with the pan‐genome. We demonstrate the potential of this unified framework for genetic analysis of various melon traits, including rind color intensity and pattern, fruit sugar content, and resistance to fungal diseases. We anticipate that utilization of this integrated resource will enhance genetic dissection of important traits and accelerate melon breeding.
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