Selective egg cell polyspermy bypasses the triploid block.

A. thaliana developmental biology egg cell plant biology plant reproduction polyploidization polyspermy triploid block

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
06 02 2020
Historique:
received: 22 10 2019
accepted: 22 12 2019
entrez: 7 2 2020
pubmed: 7 2 2020
medline: 24 4 2021
Statut: epublish

Résumé

Polyploidization, the increase in genome copies, is considered a major driving force for speciation. We have recently provided the first direct in planta evidence for polyspermy induced polyploidization. Capitalizing on a novel Ever since Darwin published his most famous book on the theory of evolution, scientists have sought to identify the mechanisms that drive the formation of new species. This is especially true for plant biologists who have long been fascinated by the extraordinary diversity of flowering plants.Many species of flowering plant first evolved after a dramatic increase in the DNA content of an individual plant, a process termed polyploidization. Most explanations for polyploidization involve a pollen grain making sperm that mistakenly contain two sets of chromosomes rather than one. Yet, it is difficult to reconcile this explanation with an important aspect of plant reproduction – the so-called “triploid block”.Fertilization in flowering plants is more complicated than in animals. While one sperm fertilizes the egg cell to make the plant embryo, a second sperm from the same pollen grain must fertilize another cell to form the endosperm, the tissue that will nourish the embryo as it develops. This means that sperm with twice the normal number of chromosomes would affect the DNA content of both the embryo and the endosperm. Yet, an endosperm that receives extra paternal DNA typically halts the development of the seed via a process known as the triploid block, meaning it was not clear how often this process would actually result in a polyploid plant.In 2017, researchers reported that plants can, on rare occasions, generate polyploid offspring via a different route: the fertilization of one egg with two sperm rather than one. Now, Mao et al. – who include several researchers involved in the 2017 study – show that this process, termed “polyspermy”, can introduce extra copies of DNA into just the egg cell, meaning it can bypass the triploid block of the endosperm.The experiments involved a model plant called Arabidopsis, and a screen of over 55,000 seeds identified about a dozen with embryos that had three parents, one mother and two fathers. Notably, most of these three-parent embryos developed in seeds that contained endosperm with the regular number of chromosomes and hence escaped the triploid block.These new results show that polyspermy provides plants with a means to essentially sneak extra copies of DNA ‘behind the back’ of the DNA-sensitive endosperm and into the next generation. They also give new insight in how polyploidization may have shaped the evolution of flowering plants and have important implications for agriculture where the breeding of new “hybrid” crops has often been limited by incompatibilities in the endosperm.

Autres résumés

Type: plain-language-summary (eng)
Ever since Darwin published his most famous book on the theory of evolution, scientists have sought to identify the mechanisms that drive the formation of new species. This is especially true for plant biologists who have long been fascinated by the extraordinary diversity of flowering plants.Many species of flowering plant first evolved after a dramatic increase in the DNA content of an individual plant, a process termed polyploidization. Most explanations for polyploidization involve a pollen grain making sperm that mistakenly contain two sets of chromosomes rather than one. Yet, it is difficult to reconcile this explanation with an important aspect of plant reproduction – the so-called “triploid block”.Fertilization in flowering plants is more complicated than in animals. While one sperm fertilizes the egg cell to make the plant embryo, a second sperm from the same pollen grain must fertilize another cell to form the endosperm, the tissue that will nourish the embryo as it develops. This means that sperm with twice the normal number of chromosomes would affect the DNA content of both the embryo and the endosperm. Yet, an endosperm that receives extra paternal DNA typically halts the development of the seed via a process known as the triploid block, meaning it was not clear how often this process would actually result in a polyploid plant.In 2017, researchers reported that plants can, on rare occasions, generate polyploid offspring via a different route: the fertilization of one egg with two sperm rather than one. Now, Mao et al. – who include several researchers involved in the 2017 study – show that this process, termed “polyspermy”, can introduce extra copies of DNA into just the egg cell, meaning it can bypass the triploid block of the endosperm.The experiments involved a model plant called Arabidopsis, and a screen of over 55,000 seeds identified about a dozen with embryos that had three parents, one mother and two fathers. Notably, most of these three-parent embryos developed in seeds that contained endosperm with the regular number of chromosomes and hence escaped the triploid block.These new results show that polyspermy provides plants with a means to essentially sneak extra copies of DNA ‘behind the back’ of the DNA-sensitive endosperm and into the next generation. They also give new insight in how polyploidization may have shaped the evolution of flowering plants and have important implications for agriculture where the breeding of new “hybrid” crops has often been limited by incompatibilities in the endosperm.

Identifiants

pubmed: 32027307
doi: 10.7554/eLife.52976
pii: 52976
pmc: PMC7004562
doi:
pii:

Substances chimiques

RNA, Messenger 0

Banques de données

GEO
['GSE130186']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : H2020 European Research Council
ID : 646644
Organisme : Deutsche Forschungsgemeinschaft
ID : GR 3526/8

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2020, Mao et al.

Déclaration de conflit d'intérêts

YM, AG, TN, PV, TB, DT, DV, IG No competing interests declared, RG The authors declare that they have filed a patent based on this work (EP3485020 A1, CN109790546, US2019159417 A1).

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Auteurs

Yanbo Mao (Y)

Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany.

Alexander Gabel (A)

Institute of Computer Science, Martin Luther University Halle-Wittenberg, Halle, Germany.

Thomas Nakel (T)

Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany.

Prisca Viehöver (P)

Faculty of Biology, Bielefeld University, Bielefeld, Germany.
Center for Biotechnology, Bielefeld University, Bielefeld, Germany.

Thomas Baum (T)

Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany.

Dawit Girma Tekleyohans (DG)

Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany.

Dieu Vo (D)

Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany.

Ivo Grosse (I)

Institute of Computer Science, Martin Luther University Halle-Wittenberg, Halle, Germany.

Rita Groß-Hardt (R)

Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany.

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