Pan-genome analysis sheds light on structural variation-based dissection of agronomic traits in melon crops.

Sweetness and appearance of fresh fruits are key palatable and preference attributes for consumers and are often controlled by multiple genes. However, fine-mapping the key loci or genes of interest by single genome-based genetic analysis is challenging. Herein, we present the chromosome-level genome assembly of 1 landrace melon accession (Cucumis melo ssp. agrestis) with wild morphologic features and thus construct a melon pan-genome atlas via integrating sequenced melon genome datasets. Our comparative genomic analysis reveals a total of 3.4 million genetic variations, of which the presence/absence variations (PAVs) are mainly involved in regulating the function of genes for sucrose metabolism during melon domestication and improvement. We further resolved several loci that are accountable for sucrose contents, flesh color, rind stripe, and suture using a structural variation (SV)-based genome-wide association study. Furthermore, via bulked segregation analysis (BSA)-seq and map-based cloning, we uncovered that a single gene, (CmPIRL6), determines the edible or inedible characteristics of melon fruit exocarp. These findings provide important melon pan-genome information and provide a powerful toolkit for future pan-genome-informed cultivar breeding of melon.

Allelic variations of ClACO gene improve nitrogen uptake via ethylene-mediated root architecture in watermelon.

KEY MESSAGE: The ClACO gene encoding 1-aminocyclopropane-1-carboxylate oxidase enabled highly efficient 15N uptake in watermelon. Nitrogen is one of the most essential nutrient elements that play a pivotal role in regulating plant growth and development for crop productivity. Elucidating the genetic basis of high nitrogen uptake is the key to improve nitrogen use efficiency for sustainable agricultural productivity. Whereas previous researches on nitrogen absorption process are mainly focused on a few model plants or crops. To date, the causal genes that determine the efficient nitrogen uptake of watermelon have not been mapped and remains largely unknown. Here, we fine-mapped the 1-aminocyclopropane-1-carboxylate oxidase (ClACO) gene associated with nitrogen uptake efficiency in watermelon via bulked segregant analysis (BSA). The variations in the ClACO gene led to the changes of gene expression levels between two watermelon accessions with different nitrogen uptake efficiencies. Intriguingly, in terms of the transcript abundance of ClACO, it was concomitant with significant differences in ethylene evolutions in roots and root architectures between the two accessions and among the different genotypic offsprings of the recombinant BC2F1(ZJU132)-18. These findings suggest that ethylene as a negative regulator altered nitrogen uptake efficiency in watermelon by controlling root development. In conclusion, our current study will provide valuable target gene for precise breeding of 'green' watermelon varieties with high-nitrogen uptake efficiencies.

An allelic variant in the ACS7 gene promotes primary root growth in watermelon.

KEY MESSAGE: Gene mining in a C. lanatus × C. amarus population revealed one gene, ACS7, linked to primary root elongation in watermelon. Watermelon is a xerophytic crop characterized by a long primary root and robust lateral roots. Therefore, watermelon serves as an excellent model for studying root elongation and development. However, the genetic mechanism underlying the primary root elongation in watermelon remains unknown. Herein, through bulk segregant analysis we identified a genetic locus, qPRL.Chr03, controlling primary root length (PRL) using two different watermelon species (Citrullus lanatus and Citrullus amarus) that differ in their root architecture. Fine mapping revealed that xaa-Pro dipeptidase and 1-aminocyclopropane-1-carboxylate synthase 7 (ACS7) are candidate regulators of the primary root growth. Allelic variation in the delimited region among 193 watermelon accessions indicated that the long-root alleles might only exist in C. amarus. Interestingly, the discrepancy in PRL among the C. amarus accessions was clearly associated with a nonsynonymous single nucleotide polymorphism variant within the ACS7 gene. The ACS7 expression and ethylene levels in the primary root tips suggested that ethylene is a negative regulator of root elongation in watermelon, as supported by the application of 1-aminocyclopropane-1-carboxylate (ACC, the ethylene precursor) or 2-aminoethoxyvinyl glycine (AVG, an ACS inhibitor). To the best of our knowledge, these findings provide the first description of the genetic basis of root elongation in watermelon. The detected markers of the ACS7 gene will facilitate marker-assisted selection for the PRL trait to improve water and nutrient use efficacy in watermelon and beyond.

Chromosome-level genome assembly of bunching onion illuminates genome evolution and flavor formation in Allium crops.

The Allium genus is cultivated globally as vegetables, condiments, or medicinal plants and is characterized by large genomes and strong pungency. However, the genome evolution and genomic basis underlying their unique flavor formation remain poorly understood. Herein, we report an 11.27-Gb chromosome-scale genome assembly for bunching onion (A. fistulosum). The uneven bursts of long-terminal repeats contribute to diversity in genome constituents, and dispersed duplication events largely account for gene expansion in Allium genomes. The extensive duplication and differentiation of alliinase and lachrymatory factor synthase manifest as important evolutionary events during flavor formation in Allium crops. Furthermore, differential selective preference for flavor-related genes likely lead to the variations in isoalliin content in bunching onions. Moreover, we reveal that China is the origin and domestication center for bunching onions. Our findings provide insights into Allium genome evolution, flavor formation and domestication history and enable future genome-assisted breeding of important traits in these crops.