Incidence and developmental timing of endosperm failure in post-zygotic isolation between wild tomato lineages

Defective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely related species. Extensive crosses within and among three lineages of wild tomatoes (Solanum section Lycopersicon) were performed to address the incidence, devel...

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Published inAnnals of botany Vol. 121; no. 1; pp. 107 - 118
Main Authors Roth, Morgane, Florez-Rueda, Ana M, Griesser, Stephan, Paris, Margot, Städler, Thomas
Format Journal Article
LanguageEnglish
Published England Oxford University Press (OUP) 25.01.2018
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Abstract Defective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely related species. Extensive crosses within and among three lineages of wild tomatoes (Solanum section Lycopersicon) were performed to address the incidence, developmental timing and histological manifestations of hybrid seed failure. These lineages encompass different, yet fairly recent, divergence times and both allopatric and partially sympatric pairs. Mature seeds were scored visually 2 months after hand pollinations, and viable-looking seeds were assessed for germination success. Using histological sections from early-developing seeds from a sub-set of crosses, the growth of three major seed compartments (endosperm, embryo and seed coat) was measured at critical developmental stages up to 21 d after pollination, with a focus on the timing and histological manifestations of endosperm misdevelopment in abortive hybrid seeds. For two of three interspecific combinations including the most closely related pair that was also studied histologically, almost all mature seeds appeared 'flat' and proved inviable; histological analyses revealed impaired endosperm proliferation at early globular embryo stages, concomitant with embryo arrest and seed abortion in both cross directions. The third interspecific combination yielded a mixture of flat, inviable and plump, viable seeds; many of the latter germinated and exhibited near-normal juvenile phenotypes or, in some instances, hybrid necrosis and impaired growth. The overall results suggest that near-complete hybrid seed failure can evolve fairly rapidly and without apparent divergence in reproductive phenology/biology. While the evidence accrued here is largely circumstantial, early-acting disruptions of normal endosperm development are most probably the common cause of seed failure regardless of the type of endosperm (nuclear or cellular).
AbstractList Defective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely related species. Extensive crosses within and among three lineages of wild tomatoes (Solanum section Lycopersicon) were performed to address the incidence, developmental timing and histological manifestations of hybrid seed failure. These lineages encompass different, yet fairly recent, divergence times and both allopatric and partially sympatric pairs. Mature seeds were scored visually 2 months after hand pollinations, and viable-looking seeds were assessed for germination success. Using histological sections from early-developing seeds from a sub-set of crosses, the growth of three major seed compartments (endosperm, embryo and seed coat) was measured at critical developmental stages up to 21 d after pollination, with a focus on the timing and histological manifestations of endosperm misdevelopment in abortive hybrid seeds. For two of three interspecific combinations including the most closely related pair that was also studied histologically, almost all mature seeds appeared 'flat' and proved inviable; histological analyses revealed impaired endosperm proliferation at early globular embryo stages, concomitant with embryo arrest and seed abortion in both cross directions. The third interspecific combination yielded a mixture of flat, inviable and plump, viable seeds; many of the latter germinated and exhibited near-normal juvenile phenotypes or, in some instances, hybrid necrosis and impaired growth. The overall results suggest that near-complete hybrid seed failure can evolve fairly rapidly and without apparent divergence in reproductive phenology/biology. While the evidence accrued here is largely circumstantial, early-acting disruptions of normal endosperm development are most probably the common cause of seed failure regardless of the type of endosperm (nuclear or cellular).
Background and AimsDefective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely related species. Extensive crosses within and among three lineages of wild tomatoes (Solanum section Lycopersicon) were performed to address the incidence, developmental timing and histological manifestations of hybrid seed failure. These lineages encompass different, yet fairly recent, divergence times and both allopatric and partially sympatric pairs.MethodsMature seeds were scored visually 2 months after hand pollinations, and viable-looking seeds were assessed for germination success. Using histological sections from early-developing seeds from a sub-set of crosses, the growth of three major seed compartments (endosperm, embryo and seed coat) was measured at critical developmental stages up to 21 d after pollination, with a focus on the timing and histological manifestations of endosperm misdevelopment in abortive hybrid seeds.Key ResultsFor two of three interspecific combinations including the most closely related pair that was also studied histologically, almost all mature seeds appeared 'flat' and proved inviable; histological analyses revealed impaired endosperm proliferation at early globular embryo stages, concomitant with embryo arrest and seed abortion in both cross directions. The third interspecific combination yielded a mixture of flat, inviable and plump, viable seeds; many of the latter germinated and exhibited near-normal juvenile phenotypes or, in some instances, hybrid necrosis and impaired growth.ConclusionsThe overall results suggest that near-complete hybrid seed failure can evolve fairly rapidly and without apparent divergence in reproductive phenology/biology. While the evidence accrued here is largely circumstantial, early-acting disruptions of normal endosperm development are most probably the common cause of seed failure regardless of the type of endosperm (nuclear or cellular).
Background and Aims Defective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely related species. Extensive crosses within and among three lineages of wild tomatoes (Solanum section Lycopersicon) were performed to address the incidence, developmental timing and histological manifestations of hybrid seed failure. These lineages encompass different, yet fairly recent, divergence times and both allopatric and partially sympatric pairs.Methods Mature seeds were scored visually 2 months after hand pollinations, and viable-looking seeds were assessed for germination success. Using histological sections from early-developing seeds from a subset of crosses, the growth of three major seed compartments (endosperm, embryo and seed coat) was measured at critical developmental stages up to 21 d after pollination, with a focus on the timing and histological manifestations of endosperm misdevelopment in abortive hybrid seeds.Key Results For two of three interspecific combinations including the most closely related pair that was also studied histologically, almost all mature seeds appeared 'flat' and proved inviable; histological analyses revealed impaired endosperm proliferation at early globular embryo stages, concomitant with embryo arrest and seed abortion in both cross directions. The third interspecific combination yielded a mixture of flat, inviable and plump, viable seeds; many of the latter germinated and exhibited near-normal juvenile phenotypes or, in some instances, hybrid necrosis and impaired growth.Conclusions The overall results suggest that near-complete hybrid seed failure can evolve fairly rapidly and without apparent divergence in reproductive phenology/biology. While the evidence accrued here is largely circumstantial, early-acting disruptions of normal endosperm development are most probably the common cause of seed failure regardless of the type of endosperm (nuclear or cellular).
Author Roth, Morgane
Florez-Rueda, Ana M
Griesser, Stephan
Paris, Margot
Städler, Thomas
AuthorAffiliation Plant Ecological Genetics, Institute of Integrative Biology & Zurich–Basel Plant Science Center, ETH Zurich, Zurich, Switzerland
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Copyright The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Distributed under a Creative Commons Attribution 4.0 International License
The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. 2017
Copyright_xml – notice: The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
– notice: Distributed under a Creative Commons Attribution 4.0 International License
– notice: The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. 2017
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Issue 1
Keywords hybrid necrosis
post-zygotic isolation
Solanum chilense
hybrid seed failure
seed development
Endosperm
Solanum peruvianum (wild tomato)
Solanum arcanum ‘marañón’
Solanum arcanum 'marañón'
Language English
License The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
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content type line 23
Present address: Plant Developmental Genetics, Department of Plant and Microbial Biology & Zurich–Basel Plant Science Center, University of Zurich, 8008 Zurich, Switzerland
Present address: Unit of Ecology & Evolution, Department of Biology, University of Fribourg, Fribourg, Switzerland
ORCID 0000-0002-5244-4215
0000-0003-2139-2528
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Snippet Defective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely related species....
Background and AimsDefective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely...
Background and Aims Defective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely...
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StartPage 107
SubjectTerms Life Sciences
Original
Plant breeding
Vegetal Biology
Title Incidence and developmental timing of endosperm failure in post-zygotic isolation between wild tomato lineages
URI https://www.ncbi.nlm.nih.gov/pubmed/29280998
https://search.proquest.com/docview/1981051558
https://hal.science/hal-03659100
https://pubmed.ncbi.nlm.nih.gov/PMC5786209
Volume 121
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