Cargando…

ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization

The current pace of crop plant optimization is insufficient to meet future demands and there is an urgent need for novel breeding strategies. It was previously shown that plants tolerate the generation of triparental polyspermy-derived plants and that polyspermy can bypass hybridization barriers. Po...

Descripción completa

Detalles Bibliográficos
Autores principales: Mao, Yanbo, Nakel, Thomas, Erbasol Serbes, Isil, Joshi, Saurabh, Tekleyohans, Dawit G, Baum, Thomas, Groß-Hardt, Rita
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10421590/
https://www.ncbi.nlm.nih.gov/pubmed/37489742
http://dx.doi.org/10.7554/eLife.85832
_version_ 1785089015918100480
author Mao, Yanbo
Nakel, Thomas
Erbasol Serbes, Isil
Joshi, Saurabh
Tekleyohans, Dawit G
Baum, Thomas
Groß-Hardt, Rita
author_facet Mao, Yanbo
Nakel, Thomas
Erbasol Serbes, Isil
Joshi, Saurabh
Tekleyohans, Dawit G
Baum, Thomas
Groß-Hardt, Rita
author_sort Mao, Yanbo
collection PubMed
description The current pace of crop plant optimization is insufficient to meet future demands and there is an urgent need for novel breeding strategies. It was previously shown that plants tolerate the generation of triparental polyspermy-derived plants and that polyspermy can bypass hybridization barriers. Polyspermy thus has the potential to harness previously incompatible climate-adapted wild varieties for plant breeding. However, factors that influence polyspermy frequencies were not previously known. The endopeptidases ECS1 and ECS2 have been reported to prevent the attraction of supernumerary pollen tubes by cleaving the pollen tube attractant LURE1. Here, we show that these genes have an earlier function that is manifested by incomplete double fertilization in plants defective for both genes. In addition to supernumerary pollen tube attraction, ecs1 ecs2 mutants exhibit a delay in synergid disintegration, are susceptible to heterofertilization, and segregate haploid plants that lack a paternal genome contribution. Our results thus uncover ECS1 and ECS2 as the first female factors triggering the induction of maternal haploids. Capitalizing on a high-throughput polyspermy assay, we in addition show that the double mutant exhibits an increase in polyspermy frequencies. As both haploid induction and polyspermy are valuable breeding aims, our results open new avenues for accelerated generation of climate-adapted cultivars.
format Online
Article
Text
id pubmed-10421590
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-104215902023-08-12 ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization Mao, Yanbo Nakel, Thomas Erbasol Serbes, Isil Joshi, Saurabh Tekleyohans, Dawit G Baum, Thomas Groß-Hardt, Rita eLife Developmental Biology The current pace of crop plant optimization is insufficient to meet future demands and there is an urgent need for novel breeding strategies. It was previously shown that plants tolerate the generation of triparental polyspermy-derived plants and that polyspermy can bypass hybridization barriers. Polyspermy thus has the potential to harness previously incompatible climate-adapted wild varieties for plant breeding. However, factors that influence polyspermy frequencies were not previously known. The endopeptidases ECS1 and ECS2 have been reported to prevent the attraction of supernumerary pollen tubes by cleaving the pollen tube attractant LURE1. Here, we show that these genes have an earlier function that is manifested by incomplete double fertilization in plants defective for both genes. In addition to supernumerary pollen tube attraction, ecs1 ecs2 mutants exhibit a delay in synergid disintegration, are susceptible to heterofertilization, and segregate haploid plants that lack a paternal genome contribution. Our results thus uncover ECS1 and ECS2 as the first female factors triggering the induction of maternal haploids. Capitalizing on a high-throughput polyspermy assay, we in addition show that the double mutant exhibits an increase in polyspermy frequencies. As both haploid induction and polyspermy are valuable breeding aims, our results open new avenues for accelerated generation of climate-adapted cultivars. eLife Sciences Publications, Ltd 2023-07-25 /pmc/articles/PMC10421590/ /pubmed/37489742 http://dx.doi.org/10.7554/eLife.85832 Text en © 2023, Mao, Nakel et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Mao, Yanbo
Nakel, Thomas
Erbasol Serbes, Isil
Joshi, Saurabh
Tekleyohans, Dawit G
Baum, Thomas
Groß-Hardt, Rita
ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization
title ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization
title_full ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization
title_fullStr ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization
title_full_unstemmed ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization
title_short ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization
title_sort ecs1 and ecs2 suppress polyspermy and the formation of haploid plants by promoting double fertilization
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10421590/
https://www.ncbi.nlm.nih.gov/pubmed/37489742
http://dx.doi.org/10.7554/eLife.85832
work_keys_str_mv AT maoyanbo ecs1andecs2suppresspolyspermyandtheformationofhaploidplantsbypromotingdoublefertilization
AT nakelthomas ecs1andecs2suppresspolyspermyandtheformationofhaploidplantsbypromotingdoublefertilization
AT erbasolserbesisil ecs1andecs2suppresspolyspermyandtheformationofhaploidplantsbypromotingdoublefertilization
AT joshisaurabh ecs1andecs2suppresspolyspermyandtheformationofhaploidplantsbypromotingdoublefertilization
AT tekleyohansdawitg ecs1andecs2suppresspolyspermyandtheformationofhaploidplantsbypromotingdoublefertilization
AT baumthomas ecs1andecs2suppresspolyspermyandtheformationofhaploidplantsbypromotingdoublefertilization
AT großhardtrita ecs1andecs2suppresspolyspermyandtheformationofhaploidplantsbypromotingdoublefertilization