The FRK1 mitogen-activated protein kinase kinase kinase (MAPKKK) from Solanum chacoense is involved in embryo sac and pollen development

Lafleur, Édith; Kapfer, Christelle; Joly, Valentin; Liu, Yang; Tebbji, Faïza; Daigle, Caroline; Gray-Mitsumune, Madoka; Cappadocia, Mario; Nantel, André; Matton, Daniel P.

doi:10.1093/jxb/eru524

Cited by 16 publications

(21 citation statements)

References 53 publications

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“…This is also a potentially interesting model for the study of the function of RALF27. No function has yet been assigned to this member of the RALF family, which is only briefly mentioned in the literature (Lafleur et al ., ; Marmiroli and Maestri, ; Olsen et al ., ). The characterization of the role of fungal RALF27 homologues during infection may also help to elucidate the function of the host homologue.…”

Section: Discussionmentioning

confidence: 98%

Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides

Thynne

Saur

Simbaqueba

et al. 2016

Molecular Plant Pathology

104

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In this article, we describe the presence of genes encoding close homologues of an endogenous plant peptide, rapid alkalinization factor (RALF), within the genomes of 26 species of phytopathogenic fungi. Members of the RALF family are key growth factors in plants, and the sequence of the RALF active region is well conserved between plant and fungal proteins. RALF1-like sequences were observed in most cases; however, RALF27-like sequences were present in the Sphaerulina musiva and Septoria populicola genomes. These two species are pathogens of poplar and, interestingly, the closest relative to their respective RALF genes is a poplar RALF27-like sequence. RALF peptides control cellular expansion during plant development, but were originally defined on the basis of their ability to induce rapid alkalinization in tobacco cell cultures. To test whether the fungal RALF peptides were biologically active in plants, we synthesized RALF peptides corresponding to those encoded by two sequenced genomes of the tomato pathogen Fusarium oxysporum f. sp. lycopersici. One of these peptides inhibited the growth of tomato seedlings and elicited responses in tomato and Nicotiana benthamiana typical of endogenous plant RALF peptides (reactive oxygen species burst, induced alkalinization and mitogen-activated protein kinase activation). Gene expression analysis confirmed that a RALF-encoding gene in F. oxysporum f. sp. lycopersici was expressed during infection on tomato. However, a subsequent reverse genetics approach revealed that the RALF peptide was not required by F. oxysporum f. sp. lycopersici for infection on tomato roots. This study has demonstrated the presence of functionally active RALF peptides encoded within phytopathogens that harbour an as yet undetermined role in plant-pathogen interactions.

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Section: Discussionmentioning

confidence: 98%

Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides

Thynne

Saur

Simbaqueba

et al. 2016

Molecular Plant Pathology

104

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“…Among the 21 Arabidopsis MEKKs, MKKK19, -20, and -21 form a highly supported clade within the MEKK family. Paralogous MAPKKKs of this clade have been initially studied in Solanaceous species where they were coined Fertilization-Related Kinases (FRKs) from the first three characterized members in Solanum chacoense ( ScFRK1 , - 2 , and - 3 ) ( Gray-Mitsumune et al, 2006 ; O’Brien et al, 2007 ; Daigle and Matton, 2015 ; Lafleur et al, 2015 ). This clade has considerably expanded in the Solanaceae family that includes potato and tomato ( Daigle and Matton, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

The Arabidopsis Mitogen-Activated Protein Kinase Kinase Kinase 20 (MKKK20) Acts Upstream of MKK3 and MPK18 in Two Separate Signaling Pathways Involved in Root Microtubule Functions

et al. 2017

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Mitogen-activated protein kinase (MAPK) signaling networks represent important means of signal transduction in plants and other eukaryotes, controlling intracellular signaling by linking perception of environmental or developmental cues to downstream targets. In the Arabidopsis MEKK subfamily, the MKKK19, 20, and 21 form a highly supported clade with the Solanaceous Fertilization-Related Kinases. In Arabidopsis, little is known about this group, except for MKKK20, which is involved in osmotic stress. Using a directed MKKK-MKK yeast two-hybrid (Y2H) screen, MKKK20 was found to interact only with MKK3, while a MKKK20 large-scale Y2H screen retrieved MPK18 as a direct interactant. In vitro phosphorylation assays showed that MKKK20 phosphorylates both MKK3 and MPK18. However, when all three kinases are combined, no synergistic effect is observed on MPK18 phosphorylation, suggesting a direct access to MPK18, consistent with the absence of interaction between MKK3 and MPK18 in protein–protein interaction assays. Since mpk18 mutant plants were previously shown to be defective in microtubule-related functions, phenotypes of mkkk20 single and mkkk20/mpk18 double mutants were investigated to determine if MKKK20 acts upstream of MPK18. This was the case, as mkkk20 root length was shorter than WT in media containing microtubule-disrupting drugs as previously observed for mpk18 plants. Surprisingly, mkk3 plants were also similarly affected, suggesting the presence of two non-complementary pathways involved in Arabidopsis cortical microtubule function, the first including MKKK20, MKK3 and an unknown MPK; the second, a non-canonical MAPK cascade made of MKKK20 and MPK18 that bypasses the need for an MKK intermediate.

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“…Pollen viability is also severely reduced in these transgenic lines [ 47 ]. RNAi and cosuppression transgenic lines for ScFRK1 [ 48 ] and ScFRK3 (Daigle et al, unpublished results) also showed severe defects in female gametophytes due to abnormal progression through megagametogenesis, leading to embryo sac collapse. Pollen viability is also severely reduced in those mutants.…”

Section: Introductionmentioning

confidence: 99%

Genome-wide analysis of MAPKKKs shows expansion and evolution of a new MEKK class involved in solanaceous species sexual reproduction

Daigle

Matton

2015

BMC Genomics

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BackgroundMembers of the plant MAP Kinases superfamily have been mostly studied in Arabidopsis thaliana and little is known in most other species. In Solanum chacoense, a wild species close to the common potato, it had been reported that members of a specific group in the MEKK subfamily, namely ScFRK1 and ScFRK2, are involved in male and female reproductive development. Apart from these two kinases, almost nothing is known about the roles of this peculiar family.MethodsMEKKs were identified using BLAST and hidden Markov model (HMM) to build profiles using the 21 MEKKs from A. thaliana. Following protein sequence alignments, the neighbor-joining method was used to reconstruct phylogenetic trees of the MEKK subfamily. Kinase subdomains sequence logos were generated with WebLogo in order to pinpoint FRK distinct motifs. Codon alignments of the FRKs kinase subdomains and maximum-likelihood phylogenetic trees were used in the codon substitution models of the codeml program in the PAML package to detect selective pressure between FRK groups.ResultsWith the recent progress in Next-Generation Sequencing technologies, the genomes and transcriptomes of numerous plant species have been recently sequenced, giving access to a vast amount of data. With the aim of finding all members of the MEKK subfamily members in plants, we screened the genomes of 15 species from different clades of the plant kingdom. Interestingly, the whole MEKK subfamily has significantly expanded throughout evolution, especially in solanaceous species. This holds true for members of the FRK class, which have also strongly expanded and diverged.ConclusionsExpansion and rapid evolution of the FRK class members in solanaceous species support the hypothesis that they have acquired new roles, mainly in male and female reproductive development.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2228-3) contains supplementary material, which is available to authorized users.

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The FRK1 mitogen-activated protein kinase kinase kinase (MAPKKK) from Solanum chacoense is involved in embryo sac and pollen development

Abstract: HighlightThis study reveals the ScFRK1 MAP kinase kinase kinase as a novel player in male and female gametophyte development, ultimately affecting pollen tube guidance and gametophyte to sporophyte communication.

Cited by 16 publications

References 53 publications

Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides

Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides

The Arabidopsis Mitogen-Activated Protein Kinase Kinase Kinase 20 (MKKK20) Acts Upstream of MKK3 and MPK18 in Two Separate Signaling Pathways Involved in Root Microtubule Functions

Genome-wide analysis of MAPKKKs shows expansion and evolution of a new MEKK class involved in solanaceous species sexual reproduction

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