Somatic variations led to the selection of acidic and acidless orange cultivars

Authors: WANG, LUN - Huazhong Agricultural University; HUANG, YUE - Huazhong Agricultural University; LIU, ZIANG - Huazhong Agricultural University; HE, JIAXIAN - Huazhong Agricultural University; JIANG, XIAOLIN - Huazhong Agricultural University; HE, FA - Huazhong Agricultural University; LU, ZHIHAO - Huazhong Agricultural University; YANG, SHUIZHI - Hunan Academy Of Agricultural Sciences; CHEN, PENG - Hunan Academy Of Agricultural Sciences; YU, HUIWEN - Huazhong Agricultural University; ZENG, BIN - Hunan Academy Of Agricultural Sciences; KE, LINGJUN - Hunan Academy Of Agricultural Sciences; XIE, ZONGZHOU - Hunan Agricultural University; LARKIN, ROBERT - Huazhong Agricultural University; JIANG, DONG - Southwest University; MING, RAY - University Of Illinois; Buckler, Edward - Ed; XU, QIANG - Huazhong Agricultural University

Submitted to: Nature Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/11/2021
Publication Date: 6/17/2021
Citation: Wang, L., Huang, Y., Liu, Z., He, J., Jiang, X., He, F., Lu, Z., Yang, S., Chen, P., Yu, H., Zeng, B., Ke, L., Xie, Z., Larkin, R., Jiang, D., Ming, R., Buckler IV, E.S., Xu, Q. 2021. Somatic variations led to the selection of acidic and acidless orange cultivars. Nature Plants. https://doi.org/10.1038/s41477-021-00941-x.
DOI: https://doi.org/10.1038/s41477-021-00941-x

Interpretive Summary: Oranges, like many of the world’s most important fruit crops, have been clonally propagated for decades or even centuries. Clonal propagation results in the accumulation of mutations over the centuries that can provide new varieties with new flavor profiles, but the mutations can also cause increases in deleterious mutations. In this study, we used modern DNA sequencing technologies to accurately reconstruct the genomes of over 100 varieties. The analysis of these natural mutations suggested that not only were single base DNA changes common, but so were transposable element (large virus-like DNA) movements. These mutations clearly document how sweet oranges moved from South China to the Mediterranean region and eventually, to the Americas. This analysis also highlighted how these mutations have likely changed the sweetness and acidity of oranges. Overall, this study provides more information about the nature and frequency of mutations in addition to some of the key mutations involved in the evolution of modern oranges.

Technical Abstract: Somatic variations are a major source of genetic diversification in asexual plants, and underpin clonal evolution and the breeding of asexual crops. Sweet orange is a model species for studying somatic variation because it reproduces asexually through apomixis and is propagated asexually through grafting. To dissect the genomic basis of somatic variation, we de novo assembled a reference genome of sweet orange with an average of three gaps per chromosome and a N50 contig of 24.2'Mb, as well as six diploid genomes of somatic mutants of sweet oranges. We then sequenced 114 somatic mutants with an average genome coverage of 41×. Categorization of the somatic variations yielded insights into the single-nucleotide somatic mutations, structural variations and transposable element (TE) transpositions. We detected 877 TE insertions, and found TE insertions in the transporter or its regulatory genes associated with variation in fruit acidity. Comparative genomic analysis of sweet oranges from three diversity centres supported a dispersal from South China to the Mediterranean region and to the Americas. This study provides a global view on the somatic variations, the diversification and dispersal history of sweet orange and a set of candidate genes that will be useful for improving fruit taste and flavour.