Patterns of Transmission Ratio Distortion in Interspecific Lettuce Hybrids Reveal a Sex-Independent Gametophytic Barrier

A.K.J. Giesbers, E. den Boer, Jacqueline Ulen, M.P.W. van Kaauwen, R.G.F. Visser, R.E. Niks, M.J.W. Jeuken*

*Corresponding author for this work

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1 Citation (Scopus)

Abstract

Interspecific crosses can result in progeny with reduced vitality or fertility due to genetic incompatibilities between species, a phenomenon known as hybrid incompatibility (HI). HI is often caused by a bias against deleterious allele combinations, which results in transmission ratio distortion (TRD). Here, we determined the genome-wide distribution of HI between wild lettuce, Lactuca saligna, and cultivated lettuce, L. sativa, in a set of backcross inbred lines (BILs) with single introgression segments from L. saligna introgressed into a L. sativa genetic background. Almost all BILs contained an introgression segment in a homozygous state except a few BILs, for which we were able to obtain only a single heterozygous introgression. Their inbred progenies displayed severe TRD with a bias toward the L. sativa allele and complete nontransmission of the homozygous L. saligna introgression, i.e., absolute HI. These HI might be caused by deleterious heterospecific allele combinations at two loci. We used an multilocus segregating interspecific F2 population to identify candidate conspecific loci that can nullify the HI in BILs. Segregation analysis of developed double-introgression progenies showed nullification of three HI and proved that these HI are explained by nuclear pairwise incompatibilities. One of these digenic HI showed 29% reduced seed set and its pattern of TRD pointed to a sex-independent gametophytic barrier. Namely, this HI was caused by complete nontransmission of one heterospecific allele combination at the haploid stage, surprisingly in both male and female gametophytes. Our study shows that two-locus incompatibility systems contribute to reproductive barriers among Lactuca species.
Original languageEnglish
Pages (from-to)263-276
JournalGenetics
Volume211
Issue number1
DOIs
Publication statusPublished - 1 Jan 2019

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Lettuce
Alleles
Ovule
Haploidy
Pollen
Fertility
Seeds
Genome

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title = "Patterns of Transmission Ratio Distortion in Interspecific Lettuce Hybrids Reveal a Sex-Independent Gametophytic Barrier",
abstract = "Interspecific crosses can result in progeny with reduced vitality or fertility due to genetic incompatibilities between species, a phenomenon known as hybrid incompatibility (HI). HI is often caused by a bias against deleterious allele combinations, which results in transmission ratio distortion (TRD). Here, we determined the genome-wide distribution of HI between wild lettuce, Lactuca saligna, and cultivated lettuce, L. sativa, in a set of backcross inbred lines (BILs) with single introgression segments from L. saligna introgressed into a L. sativa genetic background. Almost all BILs contained an introgression segment in a homozygous state except a few BILs, for which we were able to obtain only a single heterozygous introgression. Their inbred progenies displayed severe TRD with a bias toward the L. sativa allele and complete nontransmission of the homozygous L. saligna introgression, i.e., absolute HI. These HI might be caused by deleterious heterospecific allele combinations at two loci. We used an multilocus segregating interspecific F2 population to identify candidate conspecific loci that can nullify the HI in BILs. Segregation analysis of developed double-introgression progenies showed nullification of three HI and proved that these HI are explained by nuclear pairwise incompatibilities. One of these digenic HI showed 29{\%} reduced seed set and its pattern of TRD pointed to a sex-independent gametophytic barrier. Namely, this HI was caused by complete nontransmission of one heterospecific allele combination at the haploid stage, surprisingly in both male and female gametophytes. Our study shows that two-locus incompatibility systems contribute to reproductive barriers among Lactuca species.",
author = "A.K.J. Giesbers and {den Boer}, E. and Jacqueline Ulen and {van Kaauwen}, M.P.W. and R.G.F. Visser and R.E. Niks and M.J.W. Jeuken",
year = "2019",
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doi = "10.1534/genetics.118.301566",
language = "English",
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Patterns of Transmission Ratio Distortion in Interspecific Lettuce Hybrids Reveal a Sex-Independent Gametophytic Barrier. / Giesbers, A.K.J.; den Boer, E.; Ulen, Jacqueline; van Kaauwen, M.P.W.; Visser, R.G.F.; Niks, R.E.; Jeuken, M.J.W.

In: Genetics, Vol. 211, No. 1, 01.01.2019, p. 263-276.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Patterns of Transmission Ratio Distortion in Interspecific Lettuce Hybrids Reveal a Sex-Independent Gametophytic Barrier

AU - Giesbers, A.K.J.

AU - den Boer, E.

AU - Ulen, Jacqueline

AU - van Kaauwen, M.P.W.

AU - Visser, R.G.F.

AU - Niks, R.E.

AU - Jeuken, M.J.W.

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Interspecific crosses can result in progeny with reduced vitality or fertility due to genetic incompatibilities between species, a phenomenon known as hybrid incompatibility (HI). HI is often caused by a bias against deleterious allele combinations, which results in transmission ratio distortion (TRD). Here, we determined the genome-wide distribution of HI between wild lettuce, Lactuca saligna, and cultivated lettuce, L. sativa, in a set of backcross inbred lines (BILs) with single introgression segments from L. saligna introgressed into a L. sativa genetic background. Almost all BILs contained an introgression segment in a homozygous state except a few BILs, for which we were able to obtain only a single heterozygous introgression. Their inbred progenies displayed severe TRD with a bias toward the L. sativa allele and complete nontransmission of the homozygous L. saligna introgression, i.e., absolute HI. These HI might be caused by deleterious heterospecific allele combinations at two loci. We used an multilocus segregating interspecific F2 population to identify candidate conspecific loci that can nullify the HI in BILs. Segregation analysis of developed double-introgression progenies showed nullification of three HI and proved that these HI are explained by nuclear pairwise incompatibilities. One of these digenic HI showed 29% reduced seed set and its pattern of TRD pointed to a sex-independent gametophytic barrier. Namely, this HI was caused by complete nontransmission of one heterospecific allele combination at the haploid stage, surprisingly in both male and female gametophytes. Our study shows that two-locus incompatibility systems contribute to reproductive barriers among Lactuca species.

AB - Interspecific crosses can result in progeny with reduced vitality or fertility due to genetic incompatibilities between species, a phenomenon known as hybrid incompatibility (HI). HI is often caused by a bias against deleterious allele combinations, which results in transmission ratio distortion (TRD). Here, we determined the genome-wide distribution of HI between wild lettuce, Lactuca saligna, and cultivated lettuce, L. sativa, in a set of backcross inbred lines (BILs) with single introgression segments from L. saligna introgressed into a L. sativa genetic background. Almost all BILs contained an introgression segment in a homozygous state except a few BILs, for which we were able to obtain only a single heterozygous introgression. Their inbred progenies displayed severe TRD with a bias toward the L. sativa allele and complete nontransmission of the homozygous L. saligna introgression, i.e., absolute HI. These HI might be caused by deleterious heterospecific allele combinations at two loci. We used an multilocus segregating interspecific F2 population to identify candidate conspecific loci that can nullify the HI in BILs. Segregation analysis of developed double-introgression progenies showed nullification of three HI and proved that these HI are explained by nuclear pairwise incompatibilities. One of these digenic HI showed 29% reduced seed set and its pattern of TRD pointed to a sex-independent gametophytic barrier. Namely, this HI was caused by complete nontransmission of one heterospecific allele combination at the haploid stage, surprisingly in both male and female gametophytes. Our study shows that two-locus incompatibility systems contribute to reproductive barriers among Lactuca species.

U2 - 10.1534/genetics.118.301566

DO - 10.1534/genetics.118.301566

M3 - Article

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SP - 263

EP - 276

JO - Genetics

JF - Genetics

SN - 0016-6731

IS - 1

ER -