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; Hua Xing 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

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 MuñozAgnes Hotz-Wagenblatt, Xiangjia Jack Min, Hakan Özkan, Elmira Ziya Motalebipour, Hatice Gozel, Nergiz Çoban, Nesibe Ebru Kafkas, Andrej Kilian, Hua Xing Huang, Xuanrui Lv, Kunpeng Liu, Qilin Hu, Ewelina Jacygrad, William Palmer, Richard Michelmore, Ray Ming^*

^*Corresponding author for this work

Biochemistry and Molecular Genetics

Research output: Contribution to journal › Article › peer-review

14 Scopus citations

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.

Original language	English (US)
Article number	100497
Journal	Plant Communications
Volume	4
Issue number	3
DOIs	https://doi.org/10.1016/j.xplc.2022.100497
State	Published - May 8 2023

Funding

The authors would like to thank the Scientific and Technological Research Council of Turkey (project nos. TUBITAK-TOVAG 100 O 113 and TUBITAK-TOVAG 113 O 962), the University of Çukurova Scientific Research Projects Unit (project nos. FDK-2015-3641, FDK-2015-3642, FBA-2015-4521, FBA-2015-4538, FBA-2016-5406, FBA-2016-5442, FBA-2016-5407, FDK-2017-9232, FBA-2017-8250, and FBA-2020-11957), the Ministerio de Ciencia e Innovación of Spain (project nos. AGL2009-09094 and RYC-2011-08653), the University of Granada (project no. PP2016-PIP13), and the Natural Science Foundation of Fujian Province, China (project nos. 2021J01142 and 2018J01606) for providing financial support for this research. The authors wish to thank the Gaziantep Pistachio Research Institute and University of Çukurova in Turkey for providing plant materials. The authors would like to thank the Scientific and Technological Research Council of Turkey (project nos. TUBITAK-TOVAG 100 O 113 and TUBITAK-TOVAG 113 O 962 ), the University of Çukurova Scientific Research Projects Unit (project nos. FDK-2015-3641 , FDK-2015-3642 , FBA-2015-4521 , FBA-2015-4538 , FBA-2016-5406 , FBA-2016-5442 , FBA-2016-5407 , FDK-2017-9232 , FBA-2017-8250 , and FBA-2020-11957 ), the Ministerio de Ciencia e Innovación of Spain (project nos. AGL2009-09094 and RYC-2011-08653 ), the University of Granada (project no. PP2016-PIP13 ), and the Natural Science Foundation of Fujian Province , China (project nos. 2021J01142 and 2018J01606 ) for providing financial support for this research. The authors wish to thank the Gaziantep Pistachio Research Institute and University of Çukurova in Turkey for providing plant materials.

Keywords

Pistacia vera
domestication
pistachio
reference genome
sequencing
sex chromosome

ASJC Scopus subject areas

Biotechnology
Biochemistry
Molecular Biology
Plant Science
Cell Biology

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10.1016/j.xplc.2022.100497

Cite this

Kafkas, S., Ma, X., Zhang, X., Topçu, H., Navajas-Pérez, R., Wai, C. M., Tang, H., Xu, X., Khodaeiaminjan, M., Güney, M., Paizila, A., Karcı, H., Zhang, X., Lin, J., Lin, H., Herrán, R. D. L., Rejón, C. R., García-Zea, J. A., Robles, F., ... Ming, R. (2023). Pistachio genomes provide insights into nut tree domestication and ZW sex chromosome evolution. Plant Communications, 4(3), Article 100497. https://doi.org/10.1016/j.xplc.2022.100497

@article{43c87250f2c049d18ed8f3e69da972f5,

title = "Pistachio genomes provide insights into nut tree domestication and ZW sex chromosome evolution",

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",

author = "Salih Kafkas and Xiaokai Ma and Xingtan Zhang and Hayat Top{\c c}u and Rafael Navajas-P{\'e}rez and Wai, {Ching Man} and Haibao Tang and Xuming Xu and Mortaza Khodaeiaminjan and Murat G{\"u}ney and Aibibula Paizila and Harun Karcı and Xiaodan Zhang and Jing Lin and Han Lin and Herr{\'a}n, {Roberto de la} and Rej{\'o}n, {Carmelo Ruiz} and Garc{\'i}a-Zea, {Jerson Alexander} and Francisca Robles and Mu{\~n}oz, {Coral del Val} and Agnes Hotz-Wagenblatt and Min, {Xiangjia Jack} and Hakan {\"O}zkan and Motalebipour, {Elmira Ziya} and Hatice Gozel and Nergiz {\c C}oban and Kafkas, {Nesibe Ebru} and Andrej Kilian and Huang, {Hua Xing} and Xuanrui Lv and Kunpeng Liu and Qilin Hu and Ewelina Jacygrad and William Palmer and Richard Michelmore and Ray Ming",

note = "Funding Information: The authors would like to thank the Scientific and Technological Research Council of Turkey (project nos. TUBITAK-TOVAG 100 O 113 and TUBITAK-TOVAG 113 O 962), the University of {\c C}ukurova Scientific Research Projects Unit (project nos. FDK-2015-3641, FDK-2015-3642, FBA-2015-4521, FBA-2015-4538, FBA-2016-5406, FBA-2016-5442, FBA-2016-5407, FDK-2017-9232, FBA-2017-8250, and FBA-2020-11957), the Ministerio de Ciencia e Innovaci{\'o}n of Spain (project nos. AGL2009-09094 and RYC-2011-08653), the University of Granada (project no. PP2016-PIP13), and the Natural Science Foundation of Fujian Province, China (project nos. 2021J01142 and 2018J01606) for providing financial support for this research. The authors wish to thank the Gaziantep Pistachio Research Institute and University of {\c C}ukurova in Turkey for providing plant materials. Funding Information: The authors would like to thank the Scientific and Technological Research Council of Turkey (project nos. TUBITAK-TOVAG 100 O 113 and TUBITAK-TOVAG 113 O 962 ), the University of {\c C}ukurova Scientific Research Projects Unit (project nos. FDK-2015-3641 , FDK-2015-3642 , FBA-2015-4521 , FBA-2015-4538 , FBA-2016-5406 , FBA-2016-5442 , FBA-2016-5407 , FDK-2017-9232 , FBA-2017-8250 , and FBA-2020-11957 ), the Ministerio de Ciencia e Innovaci{\'o}n of Spain (project nos. AGL2009-09094 and RYC-2011-08653 ), the University of Granada (project no. PP2016-PIP13 ), and the Natural Science Foundation of Fujian Province , China (project nos. 2021J01142 and 2018J01606 ) for providing financial support for this research. The authors wish to thank the Gaziantep Pistachio Research Institute and University of {\c C}ukurova in Turkey for providing plant materials. Publisher Copyright: {\textcopyright} 2022 The Author(s)",

year = "2023",

month = may,

day = "8",

doi = "10.1016/j.xplc.2022.100497",

language = "English (US)",

volume = "4",

journal = "Plant Communications",

issn = "2590-3462",

publisher = "Cell Press",

number = "3",

}

Kafkas, S, Ma, X, Zhang, X, Topçu, H, Navajas-Pérez, R, Wai, CM, Tang, H, Xu, X, Khodaeiaminjan, M, Güney, M, Paizila, A, Karcı, H, Zhang, X, Lin, J, Lin, H, Herrán, RDL, Rejón, CR, García-Zea, JA, Robles, F, Muñoz, CDV, Hotz-Wagenblatt, A, Min, XJ, Özkan, H, Motalebipour, EZ, Gozel, H, Çoban, N, Kafkas, NE, Kilian, A, Huang, HX, Lv, X, Liu, K, Hu, Q, Jacygrad, E, Palmer, W, Michelmore, R & Ming, R 2023, 'Pistachio genomes provide insights into nut tree domestication and ZW sex chromosome evolution', Plant Communications, vol. 4, no. 3, 100497. https://doi.org/10.1016/j.xplc.2022.100497

TY - JOUR

T1 - Pistachio genomes provide insights into nut tree domestication and ZW sex chromosome evolution

AU - Kafkas, Salih

AU - Ma, Xiaokai

AU - Zhang, Xingtan

AU - Topçu, Hayat

AU - Navajas-Pérez, Rafael

AU - Wai, Ching Man

AU - Tang, Haibao

AU - Xu, Xuming

AU - Khodaeiaminjan, Mortaza

AU - Güney, Murat

AU - Paizila, Aibibula

AU - Karcı, Harun

AU - Zhang, Xiaodan

AU - Lin, Jing

AU - Lin, Han

AU - Herrán, Roberto de la

AU - Rejón, Carmelo Ruiz

AU - García-Zea, Jerson Alexander

AU - Robles, Francisca

AU - Muñoz, Coral del Val

AU - Hotz-Wagenblatt, Agnes

AU - Min, Xiangjia Jack

AU - Özkan, Hakan

AU - Motalebipour, Elmira Ziya

AU - Gozel, Hatice

AU - Çoban, Nergiz

AU - Kafkas, Nesibe Ebru

AU - Kilian, Andrej

AU - Huang, Hua Xing

AU - Lv, Xuanrui

AU - Liu, Kunpeng

AU - Hu, Qilin

AU - Jacygrad, Ewelina

AU - Palmer, William

AU - Michelmore, Richard

AU - Ming, Ray

N1 - Funding Information: The authors would like to thank the Scientific and Technological Research Council of Turkey (project nos. TUBITAK-TOVAG 100 O 113 and TUBITAK-TOVAG 113 O 962), the University of Çukurova Scientific Research Projects Unit (project nos. FDK-2015-3641, FDK-2015-3642, FBA-2015-4521, FBA-2015-4538, FBA-2016-5406, FBA-2016-5442, FBA-2016-5407, FDK-2017-9232, FBA-2017-8250, and FBA-2020-11957), the Ministerio de Ciencia e Innovación of Spain (project nos. AGL2009-09094 and RYC-2011-08653), the University of Granada (project no. PP2016-PIP13), and the Natural Science Foundation of Fujian Province, China (project nos. 2021J01142 and 2018J01606) for providing financial support for this research. The authors wish to thank the Gaziantep Pistachio Research Institute and University of Çukurova in Turkey for providing plant materials. Funding Information: The authors would like to thank the Scientific and Technological Research Council of Turkey (project nos. TUBITAK-TOVAG 100 O 113 and TUBITAK-TOVAG 113 O 962 ), the University of Çukurova Scientific Research Projects Unit (project nos. FDK-2015-3641 , FDK-2015-3642 , FBA-2015-4521 , FBA-2015-4538 , FBA-2016-5406 , FBA-2016-5442 , FBA-2016-5407 , FDK-2017-9232 , FBA-2017-8250 , and FBA-2020-11957 ), the Ministerio de Ciencia e Innovación of Spain (project nos. AGL2009-09094 and RYC-2011-08653 ), the University of Granada (project no. PP2016-PIP13 ), and the Natural Science Foundation of Fujian Province , China (project nos. 2021J01142 and 2018J01606 ) for providing financial support for this research. The authors wish to thank the Gaziantep Pistachio Research Institute and University of Çukurova in Turkey for providing plant materials. Publisher Copyright: © 2022 The Author(s)

PY - 2023/5/8

Y1 - 2023/5/8

N2 - 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.

AB - 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.

KW - Pistacia vera

KW - domestication

KW - pistachio

KW - reference genome

KW - sequencing

KW - sex chromosome

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UR - http://www.scopus.com/inward/citedby.url?scp=85147031095&partnerID=8YFLogxK

U2 - 10.1016/j.xplc.2022.100497

DO - 10.1016/j.xplc.2022.100497

M3 - Article

C2 - 36435969

AN - SCOPUS:85147031095

SN - 2590-3462

VL - 4

JO - Plant Communications

JF - Plant Communications

IS - 3

M1 - 100497

ER -

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

Abstract

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