The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development
Abstract Background The Fertilization-related kinases (FRK) form a class that belongs to the MEKK subfamily of plant MAPKKKs. It was recently shown that FRK class kinases expanded during angiosperm evolution, reaching their maximum numbers in the lineage leading to solanaceous species and culminatin...
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| Format: | Article |
| Language: | English |
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BMC
2019-05-01
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| Series: | BMC Plant Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s12870-019-1804-0 |
| _version_ | 1828492672300482560 |
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| author | Caroline Daigle Benjamin Mazin Daniel P. Matton |
| author_facet | Caroline Daigle Benjamin Mazin Daniel P. Matton |
| author_sort | Caroline Daigle |
| collection | DOAJ |
| description | Abstract Background The Fertilization-related kinases (FRK) form a class that belongs to the MEKK subfamily of plant MAPKKKs. It was recently shown that FRK class kinases expanded during angiosperm evolution, reaching their maximum numbers in the lineage leading to solanaceous species and culminating in the Solanum genus where they account for more than 40% of the total MEKKs. The first members studied, ScFRK1 and ScFRK2 were shown to play a pivotal role in gametophyte development in the wild potato species Solanum chacoense. Results ScFRK3 is also involved in gametophyte development. ScFRK3 is expressed in developing pollen and young ovules, reaching its highest level immediately after meiosis and during the mitosis steps in both gametophytes. Hence, three independent lines of ScFRK3 RNAi mutant plants showed decreased number of seeds per fruit. We also observed an important number of degenerated embryo sac in mature ovary. Analysis of ovule development showed that most embryo sac did not enter mitosis I in ScFRK3 RNAi mutant plants. Severe lethality was also observed during male gametophyte development, pollen being arrested before mitosis I, as observed in the female gametophyte. Obvious defects in vegetative organs were not observed, emphasizing the reproductive roles of the FRK class kinases. To isolate MAP kinases acting downstream of ScFRK3, a de novo S. chacoense transcriptome from male and female reproductive organs was assembled. Of the five ScMKKs and 16 ScMPKs retrieved, only the ScMKK3 interacted with ScFRK3, while only the ScMPK13 interacted with ScMKK3, leading to an apparent single three-tiered canonical MAP kinase cascade combination involving ScFRK3-ScMKK3-ScMPK13. Conclusions The ScFRK3 MAPKKK is involved in a signaling cascade that regulates both male and female gamete development, and most probably act upstream of ScMKK3 and ScMPK13. |
| first_indexed | 2024-12-11T11:24:40Z |
| format | Article |
| id | doaj.art-dcb717ff5ca24816a8556adb40fd67c1 |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-12-11T11:24:40Z |
| publishDate | 2019-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-dcb717ff5ca24816a8556adb40fd67c12022-12-22T01:09:03ZengBMCBMC Plant Biology1471-22292019-05-0119111410.1186/s12870-019-1804-0The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte developmentCaroline Daigle0Benjamin Mazin1Daniel P. Matton2Institut de recherche en biologie végétale, Département de sciences biologiques, Université de MontréalInstitut de recherche en biologie végétale, Département de sciences biologiques, Université de MontréalInstitut de recherche en biologie végétale, Département de sciences biologiques, Université de MontréalAbstract Background The Fertilization-related kinases (FRK) form a class that belongs to the MEKK subfamily of plant MAPKKKs. It was recently shown that FRK class kinases expanded during angiosperm evolution, reaching their maximum numbers in the lineage leading to solanaceous species and culminating in the Solanum genus where they account for more than 40% of the total MEKKs. The first members studied, ScFRK1 and ScFRK2 were shown to play a pivotal role in gametophyte development in the wild potato species Solanum chacoense. Results ScFRK3 is also involved in gametophyte development. ScFRK3 is expressed in developing pollen and young ovules, reaching its highest level immediately after meiosis and during the mitosis steps in both gametophytes. Hence, three independent lines of ScFRK3 RNAi mutant plants showed decreased number of seeds per fruit. We also observed an important number of degenerated embryo sac in mature ovary. Analysis of ovule development showed that most embryo sac did not enter mitosis I in ScFRK3 RNAi mutant plants. Severe lethality was also observed during male gametophyte development, pollen being arrested before mitosis I, as observed in the female gametophyte. Obvious defects in vegetative organs were not observed, emphasizing the reproductive roles of the FRK class kinases. To isolate MAP kinases acting downstream of ScFRK3, a de novo S. chacoense transcriptome from male and female reproductive organs was assembled. Of the five ScMKKs and 16 ScMPKs retrieved, only the ScMKK3 interacted with ScFRK3, while only the ScMPK13 interacted with ScMKK3, leading to an apparent single three-tiered canonical MAP kinase cascade combination involving ScFRK3-ScMKK3-ScMPK13. Conclusions The ScFRK3 MAPKKK is involved in a signaling cascade that regulates both male and female gamete development, and most probably act upstream of ScMKK3 and ScMPK13.http://link.springer.com/article/10.1186/s12870-019-1804-0Mitogen-activated protein kinase kinase kinase (MAPKKK or MEKK)Mitogen-activated protein kinase kinase (MAPKK or MEK)Mitogen-activated protein kinase (MAPK or MPK)Signaling cascadeReproductionGametophyte |
| spellingShingle | Caroline Daigle Benjamin Mazin Daniel P. Matton The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development BMC Plant Biology Mitogen-activated protein kinase kinase kinase (MAPKKK or MEKK) Mitogen-activated protein kinase kinase (MAPKK or MEK) Mitogen-activated protein kinase (MAPK or MPK) Signaling cascade Reproduction Gametophyte |
| title | The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development |
| title_full | The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development |
| title_fullStr | The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development |
| title_full_unstemmed | The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development |
| title_short | The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development |
| title_sort | solanum chacoense fertilization related kinase 3 scfrk3 is involved in male and female gametophyte development |
| topic | Mitogen-activated protein kinase kinase kinase (MAPKKK or MEKK) Mitogen-activated protein kinase kinase (MAPKK or MEK) Mitogen-activated protein kinase (MAPK or MPK) Signaling cascade Reproduction Gametophyte |
| url | http://link.springer.com/article/10.1186/s12870-019-1804-0 |
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