Four chromosome scale genomes and a pan-genome annotation to accelerate pecan tree breeding

Authors: LOVELL, JOHN - Hudsonalpha Institute For Biotechnology; BENTLEY, NOLAN - Texas A&M University; BHATTARAI, GAURAB - University Of Georgia; JENKINS, JERRY - Hudsonalpha Institute For Biotechnology; SREEDASYAM, AVINASH - Hudsonalpha Institute For Biotechnology; ALARCON, YANINA - Samuel Roberts Noble Foundation, Inc; Bock, Clive; BOSTON, LORIBETH - Hudsonalpha Institute For Biotechnology; CARLSON, JOSEPH - Department Of Energy Joint Genome; CERVANTES, KIMBERLY - New Mexico State University; CLERMONT, KRISTEN - Oak Ridge Institute For Science And Education (ORISE); Duke, Sara; KROM, NICK - Samuel Roberts Noble Foundation, Inc; Kubenka, Keith; MAMIDI, SUJAN - Hudsonalpha Institute For Biotechnology; Mattison, Chris; MONTEROS, MARIA - Samuel Roberts Noble Foundation, Inc; Pisani, Cristina; PLOTT, CHRISTOPHER - Hudsonalpha Institute For Biotechnology; RAJASEKAR, SHAWN - University Of Arizona; RHEIN, HORMAT - New Mexico State University; ROHLA, CHARLES - Samuel Roberts Noble Foundation, Inc; SONG, MINGZHOU - New Mexico State University; ST. HILAIRE, ROLSTON - New Mexico State University; SHU, SHENGQIANG - Department Of Energy Joint Genome; WELLS, LENNY - New Mexico State University; WEBBER, JENELL - Hudsonalpha Institute For Biotechnology; HEEREMA, RICHARD - New Mexico State University; KLEIN, PATRICIA - Texas A&M University; CONNER, PATRICK - University Of Georgia; Wang, Xinwang; Grauke, Larry; GRIMWOOD, JANE - Hudsonalpha Institute For Biotechnology; SCHMUTZ, JEREMY - Hudsonalpha Institute For Biotechnology; RANDALL, JENNIFER - New Mexico State University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/7/2021
Publication Date: 7/5/2021
Citation: Lovell, J.T., Bentley, N.B., Bhattarai, G., Jenkins, J.W., Sreedasyam, A., Alarcon, Y., Bock, C., Boston, L.B., Carlson, J., Cervantes, K., Clermont, K., Duke, S., Krom, N., Kubenka, K., Mamidi, S., Mattison, C.P., Monteros, M.J., Pisani, C., Plott, C., Rajasekar, S., Rhein, H.S., Rohla, C., Song, M., St. Hilaire, R., Shu, S., Wells, L., Webber, J., Heerema, R.J., Klein, P.E., Conner, P., Wang, X., Grauke, L.J., Grimwood, J., Schmutz, J., Randall, J.J. 2021. Four chromosome scale genomes and a pan-genome annotation to accelerate pecan tree breeding. Nature Communications. 12:4125. https://doi.org/10.1038/s41467-021-24328-w.
DOI: https://doi.org/10.1038/s41467-021-24328-w

Interpretive Summary: The hickory genus Carya is a major component of the forests of North America as a member of the Oak-hickory forest ecosystem. Hickory trees were important to the first humans (Amerindians) who inhabited the continent as glaciers retreated at the end of the last Ice Age. Nuts from the pecan tree (Carya illinoinensis) became so important as food for some Amerindian tribes that stands of trees were claimed as tribal property by use as burial grounds. Amerindian use of pecans was recorded by the first European explorers on the continent. Stands of “native” pecan trees from the original forest were used by early European and later American settlers, contributing to pecan’s development as the most economically valuable native nut tree crop. Recent studies show that pecan kernels are very high in valuable oils, making them a “heart-healthy” food. The selection of individual trees for propagation by grafting led to a vibrant nursery industry as well as to regional cultural systems to protect the crop for harvest and sale. A pecan breeding program was started by USDA in the early 1900s, and has been followed by state breeding programs, as well as international efforts. USDA began a living collection of pecan and hickory trees to ensure their availability for use in breeding, and to conserve the valuable genetic diversity available across the wide geographic range. Breeding and selecting improved trees requires much time and special equipment. The process of breeding would be improved by understanding the genes that control valuable traits like disease and insect resistance, consistent nut production, reduced tree size, and improved taste and nutritional value. A team of national researchers has been working to create full genome sequence “maps” of four pecan selections (‘Elliott’, ‘Lakota’, ‘Oaxaca’, and ‘Pawnee’). The four selections were chosen to represent genetic diversity across geographic range in order to capture evidence of mixing between pecans and hickories in different regions over time. This paper reports new techniques that contributed to the success of those four genome sequences. The report tells how special pecan trees are, as a group, in their genetic structure. It gives evidence of mixing between pecan trees and other hickories. It shows how some of the genetic diversity can be related to improved performance. This information will allow many people in different areas to work together more effectively, using a wider group of parent trees for breeding and allowing faster selection. This will benefit the US pecan industry and nut consumers.

Technical Abstract: Genome-enabled biotechnologies have the potential to accelerate breeding efforts in long-lived perennial crop species. Despite the transformative potential of molecular tools in pecan and other outcrossing tree species, highly heterozygous genomes and histories of interspecific hybridization have constrained efforts to exploit trait-associated markers and other molecular breeding tools. Indeed, genetic diversity and presence-absence gene content in pecan are neither captured by typical haploid genome assemblies nor a single reference genome. To overcome these constraints to current pecan breeding, we have constructed de novo diploid genomes of four outbred genotypes spanning the diversity of cultivated pecan, including a PacBio CCS chromosome-scale assembly of both haplotypes of the outbred ‘Pawnee’ cultivar genome. Comparative analysis and a pan-genome integration revealed substantial and likely adaptive interspecific genomic introgressions, including an over-retained haplotype introgressed from bitternut hickory into pecan breeding pedigrees. We then leveraged the pan-genome presence-absence and functional variant database between the two outbred haplotypes of the ‘Lakota’ genome to identify candidate genes for pathogen resistance.