Sex determination by Two Y-linked genes in garden asparagus

Alex Harkess; Kun Huang; Ron van der Hulst; Bart Tissen; Jeffrey L. Caplan; Aakash Koppula; Mona Batish; Blake C. Meyers; Jim Leebens-Mack

doi:10.1105/tpc.19.00859

Sex determination by Two Y-linked genes in garden asparagus

Alex Harkess, Kun Huang, Ron van der Hulst, Bart Tissen, Jeffrey L. Caplan, Aakash Koppula, Mona Batish, Blake C. Meyers, Jim Leebens-Mack

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58 Scopus citations

Abstract

The origin and early evolution of sex chromosomes have been hypothesized to involve the linkage of factors with antagonistic effects on male and female function. Garden asparagus (Asparagus officinalis) is an ideal species to investigate this hypothesis, as the X and Y chromosomes are cytologically homomorphic and evolved from an ancestral autosome pair in association with a shift from hermaphroditism to dioecy. Mutagenesis screens paired with single-molecule fluorescence in situ hybridization directly implicate Y-specific genes that respectively suppress female (pistil) development and are necessary for male (anther) development. Comparison of contiguous X and Y chromosome assemblies shows that hemizygosity underlies the loss of recombination between the genes suppressing female organogenesis (SUPPRESSOR OF FEMALE FUNCTION) and promoting male function (TAPETAL DEVELOPMENT AND FUNCTION1 [aspTDF1]). We also experimentally demonstrate the function of aspTDF1. These findings provide direct evidence that sex chromosomes can function through linkage of two sex determination genes.

Original language	English
Pages (from-to)	1790-1796
Number of pages	7
Journal	Plant Cell
Volume	32
Issue number	6
DOIs	https://doi.org/10.1105/tpc.19.00859
State	Published - Jun 2020

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title = "Sex determination by Two Y-linked genes in garden asparagus",

abstract = "The origin and early evolution of sex chromosomes have been hypothesized to involve the linkage of factors with antagonistic effects on male and female function. Garden asparagus (Asparagus officinalis) is an ideal species to investigate this hypothesis, as the X and Y chromosomes are cytologically homomorphic and evolved from an ancestral autosome pair in association with a shift from hermaphroditism to dioecy. Mutagenesis screens paired with single-molecule fluorescence in situ hybridization directly implicate Y-specific genes that respectively suppress female (pistil) development and are necessary for male (anther) development. Comparison of contiguous X and Y chromosome assemblies shows that hemizygosity underlies the loss of recombination between the genes suppressing female organogenesis (SUPPRESSOR OF FEMALE FUNCTION) and promoting male function (TAPETAL DEVELOPMENT AND FUNCTION1 [aspTDF1]). We also experimentally demonstrate the function of aspTDF1. These findings provide direct evidence that sex chromosomes can function through linkage of two sex determination genes.",

author = "Alex Harkess and Kun Huang and {van der Hulst}, Ron and Bart Tissen and Caplan, {Jeffrey L.} and Aakash Koppula and Mona Batish and Meyers, {Blake C.} and Jim Leebens-Mack",

note = "Funding Information: Plant material for microscopy was shared by Neil Stone (University of California, Riverside). Funding for this work was provided by the National Science Foundation (NSF Doctoral Dissertation Improvement Grant Program 1501589 to J.L.M. and A.H. and Plant Genome Research Program grant 1611853 to A.H.). Microscopy equipment was acquired with a shared instrumentation NSF grant S10 OD016361, and access supported by grant IIA-1301765.SupportwasalsoprovidedbytheNationalInstitutesofHealth (NIH; 5DP5OD012160-05 to M.B.) and access to microscopy equipment was supported by the NIH, National Institute of General Medical Sciences (grant P20 GM103446), and the state of Delaware. Publisher Copyright: {\textcopyright} 2020 American Society of Plant Biologists. All rights reserved.",

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AU - Koppula, Aakash

AU - Batish, Mona

AU - Meyers, Blake C.

AU - Leebens-Mack, Jim

N1 - Funding Information: Plant material for microscopy was shared by Neil Stone (University of California, Riverside). Funding for this work was provided by the National Science Foundation (NSF Doctoral Dissertation Improvement Grant Program 1501589 to J.L.M. and A.H. and Plant Genome Research Program grant 1611853 to A.H.). Microscopy equipment was acquired with a shared instrumentation NSF grant S10 OD016361, and access supported by grant IIA-1301765.SupportwasalsoprovidedbytheNationalInstitutesofHealth (NIH; 5DP5OD012160-05 to M.B.) and access to microscopy equipment was supported by the NIH, National Institute of General Medical Sciences (grant P20 GM103446), and the state of Delaware. Publisher Copyright: © 2020 American Society of Plant Biologists. All rights reserved.

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N2 - The origin and early evolution of sex chromosomes have been hypothesized to involve the linkage of factors with antagonistic effects on male and female function. Garden asparagus (Asparagus officinalis) is an ideal species to investigate this hypothesis, as the X and Y chromosomes are cytologically homomorphic and evolved from an ancestral autosome pair in association with a shift from hermaphroditism to dioecy. Mutagenesis screens paired with single-molecule fluorescence in situ hybridization directly implicate Y-specific genes that respectively suppress female (pistil) development and are necessary for male (anther) development. Comparison of contiguous X and Y chromosome assemblies shows that hemizygosity underlies the loss of recombination between the genes suppressing female organogenesis (SUPPRESSOR OF FEMALE FUNCTION) and promoting male function (TAPETAL DEVELOPMENT AND FUNCTION1 [aspTDF1]). We also experimentally demonstrate the function of aspTDF1. These findings provide direct evidence that sex chromosomes can function through linkage of two sex determination genes.

AB - The origin and early evolution of sex chromosomes have been hypothesized to involve the linkage of factors with antagonistic effects on male and female function. Garden asparagus (Asparagus officinalis) is an ideal species to investigate this hypothesis, as the X and Y chromosomes are cytologically homomorphic and evolved from an ancestral autosome pair in association with a shift from hermaphroditism to dioecy. Mutagenesis screens paired with single-molecule fluorescence in situ hybridization directly implicate Y-specific genes that respectively suppress female (pistil) development and are necessary for male (anther) development. Comparison of contiguous X and Y chromosome assemblies shows that hemizygosity underlies the loss of recombination between the genes suppressing female organogenesis (SUPPRESSOR OF FEMALE FUNCTION) and promoting male function (TAPETAL DEVELOPMENT AND FUNCTION1 [aspTDF1]). We also experimentally demonstrate the function of aspTDF1. These findings provide direct evidence that sex chromosomes can function through linkage of two sex determination genes.

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Sex determination by Two Y-linked genes in garden asparagus

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