The genome sequence of segmental allotetraploid peanut Arachis hypogaea

Authors: BERTIOLI, D - University Of Georgia; JENKINS, J - Department Of Energy; CLEVENGER, J - University Of Georgia; DUDCHENKO, O - Baylor College Of Medicine; GAO, D - University Of Georgia; SEIJO, G - Universidad National Del Nordeste; LEAL-BERTIOLI, S - University Of Georgia; REN, L - Iowa State University; FARMER, A - National Center For Genome Resources; PANDEY, M - International Crops Research Institute For Semi-Arid Tropics (ICRISAT) - India; SAMOLUK, SERGIO - Universidad National Del Nordeste; ABERNATHY, BRIAN - University Of Georgia; AGARWAL, GAURAV - University Of Georgia; BALLEN-TABORDA, CAROLINA - University Of Georgia; CAMERON, CONNOR - National Center For Genome Resources; CAMPBELL, JACQUELINE - Iowa State University; CHAVARRO, CAROLINA - University Of Georgia; CHITIKINENI, ANNAPURNA - International Crops Research Institute For Semi-Arid Tropics (ICRISAT) - India; CHU, YE - University Of Georgia; DASH, SUDHANSU - National Center For Genome Resources; EL BAIDOURI, MOAINE - Universite De Perpignan; Guo, Baozhu; HUANG, WEI - Iowa State University; KIM, KYUNG - University Of Georgia; KORANI, WALID - University Of Georgia; LANCIANO, SOPHIE - Universite De Perpignan; LUI, CHRISTOPHER - Baylor College Of Medicine; MIROUZE, MARIE - Universite De Perpignan; MORETZSOHN, MARCIO - Kazusa Dna Research Institute; PHAM, MELANIE - Baylor College Of Medicine; SHIN, JIN - University Of Georgia; SHIRASAWA, KENTA - Kazusa Dna Research Institute; SINHAROY, SENJUTI - National Institute Of Plant Genome Research; SREEDASYAM, AVINASH - Hudsonalpha Institute For Biotechnology; Weeks, Nathan; ZHANG, XINYOU - Henan Agricultural University; ZHENG, ZHENG - Henan Agricultural University; SUN, ZIQI - Henan Agricultural University; FROENICKE, LUTZ - University Of California, Davis; AIDEN, EREZ - Baylor College Of Medicine; MICHELMORE, RICHARD - University Of California, Davis; VARSHNEY, RAJEEV - International Crops Research Institute For Semi-Arid Tropics (ICRISAT) - India; Holbrook, Carl - Corley; CANNON, ETHALINDA - Iowa State University; Scheffler, Brian; GRIMWWOOD, JANE - Hudsonalpha Institute For Biotechnology; OZIAS-AKINS, PEGGY - University Of Georgia; Cannon, Steven; JACKSON, SCOTT - University Of Georgia; SCHMUTZ, JEREMY - Hudsonalpha Institute For Biotechnology

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/28/2019
Publication Date: 5/1/2019
Citation: Bertioli, D.J., Jenkins, J., Clevenger, J., Dudchenko, O., Gao, D., Seijo, G., Leal-Bertioli, S., Ren, L., Farmer, A., Pandey, M., Samoluk, S.S., Abernathy, B., Agarwal, G., Ballen-Taborda, C., Cameron, C., Campbell, J., Chavarro, C., Chitikineni, A., Chu, Y., Dash, S., El Baidouri, M., Guo, B., Huang, W., Kim, K.D., Korani, W., Lanciano, S., Lui, C.G., Mirouze, M., Moretzsohn, M.C., Pham, M., Shin, J.H., Shirasawa, K., Sinharoy, S., Sreedasyam, A., Weeks, N.T., Zhang, X., Zheng, Z., Sun, Z., Froenicke, L., Aiden, E.L., Michelmore, R., Varshney, R.K., Holbrook Jr, C.C., Cannon, E.K., Scheffler, B.E., Grimwwood, J., Ozias-Akins, P., Cannon, S.B., Jackson, S.A., Schmutz, J. 2019. The genome sequence of segmental allotetraploid peanut Arachis hypogaea. Nature Genetics. 51:877-884. https://doi.org/10.1038/s41588-019-0405-z.
DOI: https://doi.org/10.1038/s41588-019-0405-z

Interpretive Summary: Peanut is an important food crop (annual production of ~44 million tons worldwide). Almost all related species are diploid (two sets of chromosomes; mostly 2n = 2x = 20), but cultivated peanuts we planted at modern time in the farmers field are polyploid. It has two sets of chromosome, one from each of the ancestral diploid peanut: a type of polyploid termed an allotetraploid (AABB type genome; 2n = 4x = 40). Here, using the much longer-read DNA sequencing data obtained with PacBio and Hi-C technologies, we report the complete chromosome-scale genome sequence of cultivated peanut Tifrunner, a runner-type peanut. We also characterize the genomes of a diverse selection of cultivated peanuts, together with its wild counterpart, Arachis monticola, and induced allotetraploid hybrids derived from the ancestral diploid peanuts. We are able to quantify genetic recombination between the component A and B subgenomes. We show how this can generate morphological variation and how it provides a diversifying force in evolution of the genome of cultivated peanuts, providing variation upon which selection can act, and helped favor cultivated peanuts over its diploid relatives during the process of domestication. All these sequencing data will provide the resources and tools for genetic improvement of peanut quality/yield and disease resistance through molecular breeding and selection.

Technical Abstract: Like many other crops cultivated peanut (Arachis hypogaea L.) is a polyploid of hybrid origin, and has essentially complete sets of chromosomes from two ancestral species. Here we report the genome sequence of peanut and show that after its polyploid origin, the genome has evolved through mobile element activity, deletions and, most notably, by the flow of genetic information between corresponding chromosomes derived from the different ancestors (homeologous recombination). Uniformity of some of the patterns of recombination favors a single origin for cultivated peanut and its wild counterpart A. monticola. However, through much of the genome, homeologous recombination has created diversity. Using new polyploidy hybrids made from the ancestral species, we show how this can generate phenotypic change: spontaneous changes of flower color. This flow of genetic information between ancestral genomes is influenced by chromosome structures and is biased in different ways in different genome regions. Homeologous recombination is ongoing and is orders of magnitude more frequent than spontaneous mutation. It seems likely that this mechanism, which creates genetic diversity, helped favor the domestication of the polyploid A. hypogaea over other diploid Arachis species cultivated by humans.