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

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

doi:10.1016/j.xplc.2022.100497

Cited by 15 publications

(5 citation statements)

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“…However, the genetic regulation of dioecy varies widely across taxa. In XY systems, the male is the heterogametic sex, such as in mammals (Painter, 1921), Drosophila (McKee & Karpen, 1990), and Asparagus (Harkess et al ., 2020), while in ZW systems, the female is heterogametic, as in birds (Irwin, 2018) and pistachio ( Pistacia vera L.) (Kafkas et al ., 2022). Other, less common, examples of sex inheritance include the UV system in bryophytes where the gametophyte is the dominant generation, in Apis where males are hemizygous at the csd locus and females are homozygous (Cho et al ., 2006), and environmentally determined sexes in reptiles (Bachtrog et al ., 2014).…”

Section: Introductionmentioning

confidence: 99%

Structural variation of a sex‐linked region confers monoecy and implicates GATA15 as a master regulator of sex in Salix purpurea

et al. 2023

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The Salicaceae, including Populus and Salix, are dioecious perennials that utilize different sex determination systems. This family provides a useful system to better understand the evolution of dioecy and sex chromosomes.Here, a rare monoecious genotype of Salix purpurea, 94003, was self-and cross-pollinated and progeny sex ratios were used to test hypotheses on possible mechanisms of sex determination. To delimit genomic regions associated with monoecious expression, the 94003 genome sequence was assembled and DNA-and RNA-Seq of progeny inflorescences was performed.Based on alignments of progeny shotgun DNA sequences to the haplotype-resolved monoecious 94003 genome assembly and reference male and female genomes, a 1.15 Mb sexlinked region on Chr15W was confirmed to be absent in monecious plants. Inheritance of this structural variation is responsible for the loss of a male-suppressing function in what would otherwise be genetic females (ZW), resulting in monoecy (ZW H or WW H ), or lethality, if homozygous (W H W H ).We present a refined, two-gene sex determination model for Salix purpurea, mediated by ARR17 and GATA15 that is different from the single-gene ARR17-mediated system in the related genus Populus.

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Section: Introductionmentioning

confidence: 99%

Structural variation of a sex‐linked region confers monoecy and implicates GATA15 as a master regulator of sex in Salix purpurea

et al. 2023

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“…3C, D , and Linkage Mapping below) or some degree of chimeric misassembly on chromosomes. To ensure consistency with established nomenclature, chromosomes were named based on alignment and synteny to P. vera ( Kafkas et al 2022 ).…”

Section: Resultsmentioning

confidence: 99%

“…2004 ). Based on the alignment of each species to a genome assembly of P. vera ( Kafkas et al 2022 ) entire chromosomal scaffolds were reverse complemented using revcomp and named to match the existing chromosomal nomenclature for P. vera . In the case of P. atlantica , 2 chromosomal scaffolds showed a 2:1 relationship to a single chromosomal scaffold (Chromosome 14) in P. integerrima and P. vera , which we designated Chromosome 14.1 and 14.2.…”

Section: Methodsmentioning

confidence: 99%

Genome assembly and association tests identify interacting loci associated with vigor, precocity, and sex in interspecific pistachio rootstocks

Palmer

Jacygrad

Sagayaradj

et al. 2022

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Understanding the basis of hybrid vigor remains a key question in crop breeding and improvement, especially for rootstock development where F1 hybrids are extensively utilized. Full-sibling UCB-1 F1 seedling rootstocks are widely planted in commercial pistachio orchards that are generated by crossing two highly heterozygous outbreeding parental trees of Pistacia atlantica (female) and P. integerrima (male). This results in extensive phenotypic variability, prompting costly removal of low-yielding small trees. To identify the genetic basis of this variability, we assembled chromosome-scale genome assemblies of the parental trees of UCB-1. We genotyped 960 UCB-1 trees in an experimental orchard for which we also collected multi-year phenotypes. We genotyped an additional 1,358 rootstocks in six commercial pistachio orchards and collected single-year tree size data. Genome-wide single marker association tests identified loci associated with tree size and shape, sex, and precocity. In the experimental orchard, we identified multiple trait-associated loci and a strong candidate for ZZ/ZW sex chromosomes. We found significant marker associations unique to different traits and to early vs. late phenotypic measures of the same trait. We detected two loci strongly associated with rootstock size in commercial orchards. Pseudo-testcross classification of markers demonstrated that the trait-associated alleles for each locus were segregating in the gametes of opposite parents. These two loci interact epistatically to generate the bimodal distribution of tree size with undesirable small trees observed by growers. We identified candidate genes within these regions. These findings provide a foundational resource for marker development and genetic selection of vigorous pistachio UCB-1 rootstock.

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“…In the diecious species Pistachio, only 44 accessions were used to successfully detect sex loci. 46 In our initial analyses, simulation on different panel sizes to estimate the power for detecting true SNP-trait associations showed that when the variance explained by the locus was superior to 7%, all panels equally performed (data not shown). Hence, with a small panel, the only risk seems to not detect true SNP-trait associations for small effect loci.…”

Section: Discussionmentioning

confidence: 97%

“…Therefore even with relatively small sample sizes, it is possible to detect SNP‐trait associations, especially with qualitative or not highly quantitative traits. In the diecious species Pistachio, only 44 accessions were used to successfully detect sex loci 46 . In our initial analyses, simulation on different panel sizes to estimate the power for detecting true SNP‐trait associations showed that when the variance explained by the locus was superior to 7%, all panels equally performed (data not shown).…”

Section: Discussionmentioning

confidence: 99%

Genome‐wide association studies reveal novel loci controlling tuber flesh color and oxidative browning in Dioscorea alata

et al. 2023

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BACKGROUNDConsumers' preferences for food crops are guided by quality attributes. This study aimed at deciphering the genetic basis of quality traits, especially tuber flesh color (FC) and oxidative browning (OB) in Dioscorea alata, based on the genome‐wide association studies (GWAS) approach. The D. alata panel was planted at two locations in Guadeloupe. At harvest, the FC was scored visually as white, cream, or purple on longitudinally sliced mature tubers. The OB was scored visually as the presence or absence of browning after 15 min of exposure of the sliced samples to ambient air.RESULTSPhenotypic characterization for FC and OB of a diverse panel of D. alata genotypes highlighted significant variation within the panel and across two locations. The genotypes within the panel displayed a weak structure and could be classified into three subpopulations. GWAS identified 14 and 4 significant associations for tuber FC and OB, respectively, with phenotypic variance, explained values ranging from 7.18% to 18.04%. Allele segregation analysis at the significantly associated loci highlighted the favorable alleles for the desired traits, i.e., white FC and no OB. A total of 24 putative candidate genes were identified around the significant signals. A comparative analysis with previously reported quantitative trait loci indicated that numerous genomic regions control these traits in D. alata.CONCLUSIONOur study provides important insights into the genetic control of tuber FC and OB in D. alata. The major and stable loci can be further utilized to improve selection in breeding programs for developing new cultivars with enhanced tuber quality. © 2023 The Authors. Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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

Cited by 15 publications

References 96 publications

Structural variation of a sex‐linked region confers monoecy and implicates GATA15 as a master regulator of sex in Salix purpurea

Structural variation of a sex‐linked region confers monoecy and implicates GATA15 as a master regulator of sex in Salix purpurea

Genome assembly and association tests identify interacting loci associated with vigor, precocity, and sex in interspecific pistachio rootstocks

Genome‐wide association studies reveal novel loci controlling tuber flesh color and oxidative browning in Dioscorea alata

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