Pistachio genomes provide insights into nut tree domestication and ZW sex chromosome evolution

Salih Kafkas; Xiaokai Ma; Xingtan Zhang; Hayat Topçu; Rafael Navajas-Pérez; Ching Man Wai; Haibao Tang; Xuming Xu; Mortaza Khodaeiaminjan; Murat Güney; Aibibula Paizila; Harun Karcı; Xiaodan Zhang; Jing Lin; Han Lin; Roberto de la Herrán; Carmelo Ruiz Rejón; Jerson Alexander García-Zea; Francisca Robles; Coral Del Val Muñoz; Agnes Hotz-Wagenblatt; Xiangjia Jack Min; Hakan Özkan; Elmira Ziya Motalebipour; Hatice Gozel; Nergiz Çoban; Nesibe Ebru Kafkas; Andrej Kilian; HuaXing Huang; Xuanrui Lv; Kunpeng Liu; Qilin Hu; Ewelina Jacygrad; William Palmer; Richard Michelmore; Ray Ming

doi:10.1016/j.xplc.2022.100497

Pistachio genomes provide insights into nut tree domestication and ZW sex chromosome evolution

Plant Commun. 2023 May 8;4(3):100497. doi: 10.1016/j.xplc.2022.100497. Epub 2022 Nov 26.

Authors

Salih Kafkas¹, Xiaokai Ma², Xingtan Zhang³, Hayat Topçu⁴, Rafael Navajas-Pérez⁵, Ching Man Wai⁶, Haibao Tang³, Xuming Xu⁷, Mortaza Khodaeiaminjan⁴, Murat Güney⁴, Aibibula Paizila⁴, Harun Karcı⁴, Xiaodan Zhang⁶, Jing Lin³, Han Lin³, Roberto de la Herrán⁵, Carmelo Ruiz Rejón⁵, Jerson Alexander García-Zea⁵, Francisca Robles⁵, Coral Del Val Muñoz⁸, Agnes Hotz-Wagenblatt⁹, Xiangjia Jack Min¹⁰, Hakan Özkan¹¹, Elmira Ziya Motalebipour⁴, Hatice Gozel¹², Nergiz Çoban¹², Nesibe Ebru Kafkas⁴, Andrej Kilian¹³, HuaXing Huang³, Xuanrui Lv³, Kunpeng Liu³, Qilin Hu³, Ewelina Jacygrad¹⁴, William Palmer¹⁴, Richard Michelmore¹⁴, Ray Ming¹⁵

Affiliations

¹ Department of Horticulture, Faculty of Agriculture, University of Çukurova, Adana 01330, Turkey. Electronic address: skafkas@cu.edu.tr.
² Center for Genomics and Biotechnology, Haixia Institute of Science and Technology, School of Future Technology, Fujian Agriculture and Forestry University, Fuzhou, China; Key Laboratory of Orchid Conservation and Utilization of National Forestry and Grassland Administration, Fujian Agriculture and Forestry University, Fuzhou, China.
³ Center for Genomics and Biotechnology, Haixia Institute of Science and Technology, School of Future Technology, Fujian Agriculture and Forestry University, Fuzhou, China.
⁴ Department of Horticulture, Faculty of Agriculture, University of Çukurova, Adana 01330, Turkey.
⁵ Departamento de Genética, Facultad de Ciencias, Campus de Fuentenueva s/n, 18071 Granada, Spain.
⁶ Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
⁷ Center for Genomics and Biotechnology, Haixia Institute of Science and Technology, School of Future Technology, Fujian Agriculture and Forestry University, Fuzhou, China; Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, College of the Environment and Ecology, Xiamen University, Xiamen 361102, China.
⁸ Department of Computer Science, University of Granada, Granada, Spain; Andalusian Research Institute in Data Science and Computational Intelligence (DaSCI Institute), 18014 Granada, Spain.
⁹ German Cancer Research Center, Omics IT and Data Management Core Facility, Heidelberg, Germany.
¹⁰ Department of Biological Sciences, Youngstown State University, Youngstown, OH 44555, USA.
¹¹ Department of Field Crops, Faculty of Agriculture, University of Çukurova, Adana 01330, Turkey.
¹² Pistachio Research Institute, Şahinbey, Gaziantep 27060, Turkey.
¹³ Diversity Arrays Technology, University of Canberra, Canberra, ACT, Australia.
¹⁴ Genome Center, University of California Davis, 451 Health Sciences Drive, Davis, CA 95616, USA.
¹⁵ Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Electronic address: rayming@illinois.edu.

Abstract

Pistachio is a nut crop domesticated in the Fertile Crescent and a dioecious species with ZW sex chromosomes. We sequenced the genomes of Pistacia vera cultivar (cv.) Siirt, the female parent, and P. vera cv. Bagyolu, the male parent. Two chromosome-level reference genomes of pistachio were generated, and Z and W chromosomes were assembled. The ZW chromosomes originated from an autosome following the first inversion, which occurred approximately 8.18 Mya. Three inversion events in the W chromosome led to the formation of a 12.7-Mb (22.8% of the W chromosome) non-recombining region. These W-specific sequences contain several genes of interest that may have played a pivotal role in sex determination and contributed to the initiation and evolution of a ZW sex chromosome system in pistachio. The W-specific genes, including defA, defA-like, DYT1, two PTEN1, and two tandem duplications of six VPS13A paralogs, are strong candidates for sex determination or differentiation. Demographic history analysis of resequenced genomes suggest that cultivated pistachio underwent severe domestication bottlenecks approximately 7640 years ago, dating the domestication event close to the archeological record of pistachio domestication in Iran. We identified 390, 211, and 290 potential selective sweeps in 3 cultivar subgroups that underlie agronomic traits such as nut development and quality, grafting success, flowering time shift, and drought tolerance. These findings have improved our understanding of the genomic basis of sex determination/differentiation and horticulturally important traits and will accelerate the improvement of pistachio cultivars and rootstocks.

Keywords: Pistacia vera; domestication; pistachio; reference genome; sequencing; sex chromosome.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Domestication
Nuts
Pistacia* / genetics
Sex Chromosomes / genetics
Trees / genetics