The bottle gourd genome provides insights into Cucurbitaceae evolution and facilitates mapping of a Papaya ringspot virus resistance locus

Authors: WU, SHAN - Boyce Thompson Institute; Shamimuzzaman, Md - Shamim; SUN, HONGHE - Boyce Thompson Institute; SALSE, JEROME - Institut National De La Recherche Agronomique (INRA); SUI, XUELIAN - Fujian Agriculture And Forest University; Wilder, Alan; WU, ZUJIAN - Fujian Agriculture And Forest University; Levi, Amnon; XU, YONG - Beijing Academy Of Agricultural Sciences; Ling, Kai-Shu; FEI, ZHANGJUN - Boyce Thompson Institute

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/7/2017
Publication Date: 9/23/2017
Citation: Wu, S., Shamimuzzaman, M., Sun, H., Salse, J., Sui, X., Wilder, A.J., Wu, Z., Levi, A., Xu, Y., Ling, K., Fei, Z. 2017. The bottle gourd genome provides insights into Cucurbitaceae evolution and facilitates mapping of a Papaya ringspot virus resistance locus. Plant Journal. 92:963-975. https://doi.org/10.1111/tpj.13722.
DOI: https://doi.org/10.1111/tpj.13722

Interpretive Summary: Bottle gourd (Lagenaria siceraria) is one of the most ancient crops cultivated by humans that is widely grown in the world today, particularly in the Eastern Asian countries. There are many beneficial uses of this ancient crop plant, due largely to its various shapes of fruits that can be used for food, medicine, containers, musical instruments or decorative artifacts. In recent years, bottle gourd has also been used as an important rootstock for grafting to watermelon and other cucurbit crops to improve their disease resistance and cold tolerance. Plant diseases are a major constraint in bottle gourd production. Commercially available bottle gourd cultivars are generally susceptible to viral diseases. Papaya ringspot virus (PRSV) is one of the most destructive viruses infecting papaya and cucurbits worldwide. After screening USDA Plant Germplasm collections of bottle gourd for resistance, we previously selected and developed two lines with multiple virus resistance, including PRSV. ARS scientists collaborated with university bioinformaticians and a team of international scholars, and assembled a high-quality bottle gourd genome sequence using the inbred line USVL1VR-Ls. The high-quality reference genome of bottle gourd is a valuable resource for the improvement of this crop and for studying the evolutionary history of the Cucurbitaceae family. We demonstrate that the reported bottle gourd genome facilitates the comparative genomic analysis leading to the construction of ancestral chromosomes of Cucurbitaceae, and enables the mapping of a locus conferring PRSV resistance in bottle gourd, which is useful for marker-assisted selection in plant breeding.

Technical Abstract: Bottle gourd (Lagenaria siceraria) is an important vegetable crop as well as a rootstock for other cucurbit crops. In this study, we report a high-quality 313.4-Mb genome sequence of a bottle gourd inbred line, USVL1VR-Ls, with a scaffold N50 of 8.7 Mb and the longest of 19.0 Mb. About 98.3% of the assembled scaffolds are anchored to the 11 pseudomolecules. Comparative genomic analysis identifies nearly one-to-one chromosome-level syntenic relationship between bottle gourd and four other cucurbits, as well as linear-specific gene family expansions in bottle gourd. We reconstruct the genome of the most recent common ancestor of Cucurbitaceae, which reveals that the ancestral Cucurbitaceae karyotypes consists of 12 protochromosomes with 18,534 protogenes. The 12 protochromosomes are largely retained in the modern melon genome, while have undergone different degrees of shuffling events in other investigated cucurbit genomes. The eleven bottle gourd chromosomes derive from the ancestral Cucurbitaceae karyotypes followed by 19 chromosomal fissions and 20 fusions. The bottle gourd genome sequence has facilitated the mapping of a dominant monogenic locus, Prs, conferring Papaya ringspot virus (PRSV) resistance in bottle gourd, to a 317.8-kb region on chromosome 1. We have developed a cleaved amplified polymorphic sequence (CAPS) marker tightly linked to the Prs locus and demonstrated its potential application in marker-assisted selection of PRSV resistance in bottle gourd. This study provides insights into the paleohistory of Cucurbitaceae genome evolution, and the high-quality genome sequence of bottle gourd provides a valuable resource for plant comparative genomics studies and cucurbit improvement.