Forum
Commentary The omics era of Fusarium graminearum: opportunities and challenges How do plant pathogens colonize their hosts is a key question in the field of plant pathology. Secreted effectors, hydrolytic enzymes, toxins and even small RNAs can be deployed as the virulence or pathogenicity factors to interfere with the host immune responses. But still there are more complicated systems to command and coordinate in their arsenal. The plant pathogen Fusarium graminearum can have devastating effects causing yield loss of various cereal crops and contaminating grain with mycotoxins that are harmful to the health of humans and livestock (Rocha et al., 2005). Given the economic importance of this pathogen, F. graminearum is currently under intense investigation and is becoming a model organism to study filamentous fungal cell biology, fungal–plant interactions and secondary metabolism. In this issue of New Phytologist, Yun et al. (pp. 119–134) contribute to our knowledge of the function of the F. graminearum phosphatome in hyphal growth, development, virulence and secondary metabolism by the omics level gene deletion and phenomic description (in line with the definition of kinome, phosphatome is the complete set of phosphatases of an organism, and the reversible protein phosphorylation is involved in the regulation of various life processes). Three phosphatases were identified as negative regulators of mitogen-activated protein kinase (MAPK) pathways.
‘Although many genes are involved in fungal–plant interactions, gene redundancy and functional complementation make assigning definitive roles in virulence to be a challenging task.’
The ‘omics era’ of Fusarium graminearum The release of the Fusarium graminearum genome in 2007 (Cuomo et al., 2007) has greatly stimulated research activity on this fungus and a variety of ‘omics’ approaches have been used. Comparative genomic, transcriptomic and proteomic analyses have greatly accelerated the identification of fungal functional genes (Taylor et al., 2008; Ma et al., 2010; Zhang et al., 2012). The major Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
undertaking in fungal genomics is to investigate the function of the large number of genes identified by in silico approaches. Reverse genetics have been extensively employed to unveil the function of genes at the molecular level. Son et al. (2011) constructed a mutant library of 657 putative transcription factors which opened the curtain on large scale reverse genetics of F. graminearum. As downstream targets of signaling pathways, some transcription factors can be phosphorylated or dephosphorylated by kinases or phosphatases; functional analyses of the F. graminearum kinome and phosphatome contributed to the identification of a series of kinase or phosphatase mutants that have phenotypic changes (Wang et al., 2011; Yun et al.). Targeted gene deletion by homologous recombination in several fungi has become the most influential reverse genetics tool to identify gene function. The well annotated genome, and the efficient and tractable genetic transformation system of F. graminearum make large scale reverse genetic analyses feasible. Mutants constructed from the same progenitor have the potential to be phenotypically grouped and systematically analyzed. Yun et al. systematically characterized and annotated 82 putative phosphatase genes in F. graminearum and identified 11 essential phosphatase genes and 63 other functional phosphatase genes. Apart from the continual studies of genomics, transcriptomics, proteomics and reverse genetics, the study of fungal secondary metabolism is becoming popular due to the bio-activity of various secondary metabolites and the potential pharmaceutical benefits. Fusarium graminearum is a master in producing mycotoxins, such as aurofusarin, fusarin C, zearalenone, deoxynivalenol (DON) and its derivatives, and encodes 43 secondary metabolism key enzymes, including nonribosomal peptide synthases (NRPSs), polyketide synthases (PKSs) and terpenoid synthases (TPSs) (Ma et al., 2013). However, the majority of the potential secondary metabolites are still unknown and further investigation is needed. Of these mycotoxins, DON is an important virulence factor with tissuespecificity (Zhang et al., 2012) and host-specificity (Maier et al., 2006). Extensive molecular and genetic studies have revealed that the DON biosynthetic pathway and various signaling pathways are important for F. graminearum pathogenesis (Walter et al., 2010). In this issue of New Phytologist, Yun et al. also identified several phosphatase genes that contributed to regulation of DON production.
The investigation into the unveiling of the structure and function of complex networks of Fusarium graminearum The current concept of pathogen–host molecular interactions provides a strong conceptual framework for understanding how these organisms co-exist. Dissecting the genetic factors that influence virulence in F. graminearum has been promoted by New Phytologist (2015) 207: 1–3 1 www.newphytologist.com
2 Forum
New Phytologist
Commentary
important for pathogenesis and other responses have been identified, including the key components of MAPK, calcium, TOR and cAMP signaling pathways (Fig. 1). Although signaling pathways are often conceptualized as distinct entities responding to specific cues and affecting different biological functions, large scale reverse genetics, with mutants constructed from the same progenitor, help to group components with similar phenotypes. In their phosphatome study, Yun et al. identifed several species-specific negative regulators of the MAPK signaling pathways. In F. graminearum, three MAPK signaling pathways including the Mgv1 MAPK pathway, the Gpmk1 MAPK pathway and the Hog1 MAPK pathway (Fig. 1), have been characterized and have been shown to play important roles in various developmental and plant infection processes. Fusarium graminearum can grow in different media and infect various cereal crops using adapted strategies, thus signaling networks must play important roles. Yun et al. (in this issue of New Phytologist) and in previous work (Yu et al., 2014) identified several phosphatases as negative regulators and other
various omics studies. A future challenge in modeling the arsenal system of F. graminearum will be to unveil the signaling networks involved as the infection progresses in different hosts. In eukaryotic organisms, reversible protein or lipid phosphorylation is the main way to transfer signals; nearly one-third of the proteins are regulated via phosphorylation (Cohen, 2000). In general, c. 1–2% of predicted genes encode kinases and 0.5% encode phophatases in eukaryotes (Seshacharyulu et al., 2013). Wang et al. (2011) and Yun et al. identified 116 protein kinase (PK) genes and 82 phosphatase genes, respectively, most of which play roles in maintaining normal cellular functions, but some are involved in the signaling pathways. Mapping the signaling network has involved inferences arising from the aggregation of studies of individual pathway components from diverse experimental systems. Comparative genomics and genetic methods allow us to identify conserved pathways and specific components in different oganisms. With yeast and other fungal pathogens as references, a number of genes known to be
ht Lig
tion starva Iron
Redox status
Ambient pH
Carbon source
Receptor
FgSho1 FgBck1 FgMkk1 cascade FgSte50 FgSte11 FgSte7 cascade
Rapamycin FgFkbp12
FgTor
Fg10516
FgTap42 Mgv1 MAPK pathway
FgGpmk1
Small GTPase
FgMgv1
FgSit4
FgTap42 FgTap42 FgPpg1
espon s
es
FgSsk2 FgPbs2 cascade
FgPp2A Hog1 MAPK pathway
TOR pathway
FgRlm1 CPK1 CPK2
Unknown components
Fg09709
Ste12 FgCDC14
Fg12867
FgHog1
FgMsg5
Unknown pathways
cAMP-PKA pathway
Plant r
FgPtc3
FgMsb2
Gpmk1 MAPK pathway
rce
Receptor
FgSln1
Fg03333
Nitrogen sou
FgAreA Fg09019
FgTfc7 Other Components
Receptors Kinases Phosphatases
Cell division Ribosome biogenesis
Transcription factors Other components involved in signaling pathway
Sexual development
Secondary metabolism
Sress responses
Vegetative growth Virulence
Fig. 1 The major elements involved in the Fusarium graminearum signaling network. Environmental signals can influence the regulation of various fungal responses through signaling pathways that respond to these environmental stimuli. Three mitogen-activated protein kinase (MAPK) pathways, including Gpmk1, Mgv1 and Hog1 MAPK, play important roles in signal transduction. FgSit4 and FgPpg1 of the TOR pathway are involved in the regulation of the Mgv1 MAPK pathway via a negative regulator FgMsg5. Four phosphatases (Fg03333, Fg10516, Fg12867 and FgPtc3) act as negative regulators of MAPK pathways. Arrows and bars represent activation and repression, respectively. Figure adapted from Yu et al. (2014) and incorporates data from Yun et al. (this issue of New Phytologist, pp. 119–134). New Phytologist (2015) 207: 1–3 www.newphytologist.com
Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
New Phytologist
Commentary
components of the signaling pathway connecting various pathways into a network. These pathways receive signals from various receptors and regulate the activity of various substrates, such as transcription factors and PKs (Fig. 1). Fungal biology and fungal pathogenicity mechanisms are important aspects to study in the fungal–plant interaction. Large scale reverse genetic studies coupled with genomics and transcriptomics have significantly promoted progress in this research area. Nearly one-tenth of the genes of F. graminearum have been analyzed by Son et al. (2011), Wang et al. (2011) and Yun et al., and it is not difficult to predict that every gene of F. graminearum will be deleted or silenced and functionally analyzed in the next few years. Although many genes are involved in fungal–plant interactions, gene redundancy and functional complementation make assigning definitive roles in virulence to be a challenging task. There is a need to develop an efficient multiple-genedeletion system to generate mutants with a set of redundant genes deleted, probably with the recent CRISPRA/CAS system (Cong et al., 2013). The identification of virulence factors for a fungal pathogen is also complicated by the dependence of infection on both the pathogen and host. Two classes of pathogenicity genes including basic and specialized pathogenicity genes (Ma et al., 2013), confer F. graminearum with the ability to colonize hosts and show tissue and host specificity (Maier et al., 2006; Zhang et al., 2012), but little is known about the regulation of tissue and host specificity. There is still a long way to go and concerted efforts will need to be made to enlighten the black box of F. graminearum–host interactions.
Acknowledgements The research in W-H.T.’s laboratory is supported by the National Basic Research Program of China (2011CB100702). Lei-Jie Jia and Wei-Hua Tang* National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China (*Author for correspondence: tel +86 21 54924072; email [email protected])
Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
Forum 3
References Cohen P. 2000. The regulation of protein function by multisite phosphorylation – a 25 year update. Trends in Biochemical Sciences 25: 596–601. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819–823. Cuomo CA, G€ uldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M et al. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400–1402. Ma LJ, Geiser DM, Proctor RH, Rooney AP, O’Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K. 2013. Fusarium pathogenomics. Annual Review of Microbiology 67: 399–416. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367–373. Maier FJ, Miedaner T, Hadeler B, Felk A, Salomon S, Lemmens M, Kassner H, Schafer W. 2006. Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase (Tri5) gene in three field isolates of different chemotype and virulence. Molecular Plant Pathology 7: 449–461. Rocha O, Ansari K, Doohan FM. 2005. Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Additives & Contaminants 22: 369–378. Seshacharyulu P, Pandey P, Datta K, Batra SK. 2013. Phosphatase: PP2A structural importance, regulation and its aberrant expression in cancer. Cancer Letters 335: 9–18. Son H, Seo YS, Min K, Park AR, Lee J, Jin JM, Lin Y, Cao P, Hong SY, Kim EK et al. 2011. A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathogens 7: e1002310. Taylor RD, Saparno A, Blackwell B, Anoop V, Gleddie S, Tinker NA, Harris LJ. 2008. Proteomic analyses of Fusarium graminearum grown under mycotoxininducing conditions. Proteomics 8: 2256–2265. Walter S, Nicholson P, Doohan FM. 2010. Action and reaction of host and pathogen during Fusarium head blight disease. New Phytologist 185: 54–66. Wang C, Zhang S, Hou R, Zhao Z, Zheng Q, Xu Q, Zheng D, Wang G, Liu H, Gao X et al. 2011. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathogens 7: e1002460. Yu F, Gu Q, Yun Y, Yin Y, Xu J-R, Shim W-B, Ma Z. 2014. The TOR signaling pathway regulates vegetative development and virulence in Fusarium graminearum. New Phytologist 203: 219–232. Yun Y, Liu Z, Yin Y, Jiang J, Chen Y, Xu J-R, Ma Z. 2015. Functional analysis of the Fusarium graminearum phosphatome. New Phytologist 207: 119–134. Zhang XW, Jia LJ, Zhang Y, Jiang G, Li X, Zhang D, Tang WH. 2012. In planta stage-specific fungal gene profiling elucidates the molecular strategies of Fusarium graminearum growing inside wheat coleoptiles. Plant Cell 24: 5159–5176. Key words: fungal–plant interaction, Fusarium, mitogen-activated protein kinase (MAPK), omics, plant pathogen, secondary metabolism, signaling pathways.
New Phytologist (2015) 207: 1–3 www.newphytologist.com
Commentary The omics era of Fusarium graminearum: opportunities and challenges How do plant pathogens colonize their hosts is a key question in the field of plant pathology. Secreted effectors, hydrolytic enzymes, toxins and even small RNAs can be deployed as the virulence or pathogenicity factors to interfere with the host immune responses. But still there are more complicated systems to command and coordinate in their arsenal. The plant pathogen Fusarium graminearum can have devastating effects causing yield loss of various cereal crops and contaminating grain with mycotoxins that are harmful to the health of humans and livestock (Rocha et al., 2005). Given the economic importance of this pathogen, F. graminearum is currently under intense investigation and is becoming a model organism to study filamentous fungal cell biology, fungal–plant interactions and secondary metabolism. In this issue of New Phytologist, Yun et al. (pp. 119–134) contribute to our knowledge of the function of the F. graminearum phosphatome in hyphal growth, development, virulence and secondary metabolism by the omics level gene deletion and phenomic description (in line with the definition of kinome, phosphatome is the complete set of phosphatases of an organism, and the reversible protein phosphorylation is involved in the regulation of various life processes). Three phosphatases were identified as negative regulators of mitogen-activated protein kinase (MAPK) pathways.
‘Although many genes are involved in fungal–plant interactions, gene redundancy and functional complementation make assigning definitive roles in virulence to be a challenging task.’
The ‘omics era’ of Fusarium graminearum The release of the Fusarium graminearum genome in 2007 (Cuomo et al., 2007) has greatly stimulated research activity on this fungus and a variety of ‘omics’ approaches have been used. Comparative genomic, transcriptomic and proteomic analyses have greatly accelerated the identification of fungal functional genes (Taylor et al., 2008; Ma et al., 2010; Zhang et al., 2012). The major Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
undertaking in fungal genomics is to investigate the function of the large number of genes identified by in silico approaches. Reverse genetics have been extensively employed to unveil the function of genes at the molecular level. Son et al. (2011) constructed a mutant library of 657 putative transcription factors which opened the curtain on large scale reverse genetics of F. graminearum. As downstream targets of signaling pathways, some transcription factors can be phosphorylated or dephosphorylated by kinases or phosphatases; functional analyses of the F. graminearum kinome and phosphatome contributed to the identification of a series of kinase or phosphatase mutants that have phenotypic changes (Wang et al., 2011; Yun et al.). Targeted gene deletion by homologous recombination in several fungi has become the most influential reverse genetics tool to identify gene function. The well annotated genome, and the efficient and tractable genetic transformation system of F. graminearum make large scale reverse genetic analyses feasible. Mutants constructed from the same progenitor have the potential to be phenotypically grouped and systematically analyzed. Yun et al. systematically characterized and annotated 82 putative phosphatase genes in F. graminearum and identified 11 essential phosphatase genes and 63 other functional phosphatase genes. Apart from the continual studies of genomics, transcriptomics, proteomics and reverse genetics, the study of fungal secondary metabolism is becoming popular due to the bio-activity of various secondary metabolites and the potential pharmaceutical benefits. Fusarium graminearum is a master in producing mycotoxins, such as aurofusarin, fusarin C, zearalenone, deoxynivalenol (DON) and its derivatives, and encodes 43 secondary metabolism key enzymes, including nonribosomal peptide synthases (NRPSs), polyketide synthases (PKSs) and terpenoid synthases (TPSs) (Ma et al., 2013). However, the majority of the potential secondary metabolites are still unknown and further investigation is needed. Of these mycotoxins, DON is an important virulence factor with tissuespecificity (Zhang et al., 2012) and host-specificity (Maier et al., 2006). Extensive molecular and genetic studies have revealed that the DON biosynthetic pathway and various signaling pathways are important for F. graminearum pathogenesis (Walter et al., 2010). In this issue of New Phytologist, Yun et al. also identified several phosphatase genes that contributed to regulation of DON production.
The investigation into the unveiling of the structure and function of complex networks of Fusarium graminearum The current concept of pathogen–host molecular interactions provides a strong conceptual framework for understanding how these organisms co-exist. Dissecting the genetic factors that influence virulence in F. graminearum has been promoted by New Phytologist (2015) 207: 1–3 1 www.newphytologist.com
2 Forum
New Phytologist
Commentary
important for pathogenesis and other responses have been identified, including the key components of MAPK, calcium, TOR and cAMP signaling pathways (Fig. 1). Although signaling pathways are often conceptualized as distinct entities responding to specific cues and affecting different biological functions, large scale reverse genetics, with mutants constructed from the same progenitor, help to group components with similar phenotypes. In their phosphatome study, Yun et al. identifed several species-specific negative regulators of the MAPK signaling pathways. In F. graminearum, three MAPK signaling pathways including the Mgv1 MAPK pathway, the Gpmk1 MAPK pathway and the Hog1 MAPK pathway (Fig. 1), have been characterized and have been shown to play important roles in various developmental and plant infection processes. Fusarium graminearum can grow in different media and infect various cereal crops using adapted strategies, thus signaling networks must play important roles. Yun et al. (in this issue of New Phytologist) and in previous work (Yu et al., 2014) identified several phosphatases as negative regulators and other
various omics studies. A future challenge in modeling the arsenal system of F. graminearum will be to unveil the signaling networks involved as the infection progresses in different hosts. In eukaryotic organisms, reversible protein or lipid phosphorylation is the main way to transfer signals; nearly one-third of the proteins are regulated via phosphorylation (Cohen, 2000). In general, c. 1–2% of predicted genes encode kinases and 0.5% encode phophatases in eukaryotes (Seshacharyulu et al., 2013). Wang et al. (2011) and Yun et al. identified 116 protein kinase (PK) genes and 82 phosphatase genes, respectively, most of which play roles in maintaining normal cellular functions, but some are involved in the signaling pathways. Mapping the signaling network has involved inferences arising from the aggregation of studies of individual pathway components from diverse experimental systems. Comparative genomics and genetic methods allow us to identify conserved pathways and specific components in different oganisms. With yeast and other fungal pathogens as references, a number of genes known to be
ht Lig
tion starva Iron
Redox status
Ambient pH
Carbon source
Receptor
FgSho1 FgBck1 FgMkk1 cascade FgSte50 FgSte11 FgSte7 cascade
Rapamycin FgFkbp12
FgTor
Fg10516
FgTap42 Mgv1 MAPK pathway
FgGpmk1
Small GTPase
FgMgv1
FgSit4
FgTap42 FgTap42 FgPpg1
espon s
es
FgSsk2 FgPbs2 cascade
FgPp2A Hog1 MAPK pathway
TOR pathway
FgRlm1 CPK1 CPK2
Unknown components
Fg09709
Ste12 FgCDC14
Fg12867
FgHog1
FgMsg5
Unknown pathways
cAMP-PKA pathway
Plant r
FgPtc3
FgMsb2
Gpmk1 MAPK pathway
rce
Receptor
FgSln1
Fg03333
Nitrogen sou
FgAreA Fg09019
FgTfc7 Other Components
Receptors Kinases Phosphatases
Cell division Ribosome biogenesis
Transcription factors Other components involved in signaling pathway
Sexual development
Secondary metabolism
Sress responses
Vegetative growth Virulence
Fig. 1 The major elements involved in the Fusarium graminearum signaling network. Environmental signals can influence the regulation of various fungal responses through signaling pathways that respond to these environmental stimuli. Three mitogen-activated protein kinase (MAPK) pathways, including Gpmk1, Mgv1 and Hog1 MAPK, play important roles in signal transduction. FgSit4 and FgPpg1 of the TOR pathway are involved in the regulation of the Mgv1 MAPK pathway via a negative regulator FgMsg5. Four phosphatases (Fg03333, Fg10516, Fg12867 and FgPtc3) act as negative regulators of MAPK pathways. Arrows and bars represent activation and repression, respectively. Figure adapted from Yu et al. (2014) and incorporates data from Yun et al. (this issue of New Phytologist, pp. 119–134). New Phytologist (2015) 207: 1–3 www.newphytologist.com
Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
New Phytologist
Commentary
components of the signaling pathway connecting various pathways into a network. These pathways receive signals from various receptors and regulate the activity of various substrates, such as transcription factors and PKs (Fig. 1). Fungal biology and fungal pathogenicity mechanisms are important aspects to study in the fungal–plant interaction. Large scale reverse genetic studies coupled with genomics and transcriptomics have significantly promoted progress in this research area. Nearly one-tenth of the genes of F. graminearum have been analyzed by Son et al. (2011), Wang et al. (2011) and Yun et al., and it is not difficult to predict that every gene of F. graminearum will be deleted or silenced and functionally analyzed in the next few years. Although many genes are involved in fungal–plant interactions, gene redundancy and functional complementation make assigning definitive roles in virulence to be a challenging task. There is a need to develop an efficient multiple-genedeletion system to generate mutants with a set of redundant genes deleted, probably with the recent CRISPRA/CAS system (Cong et al., 2013). The identification of virulence factors for a fungal pathogen is also complicated by the dependence of infection on both the pathogen and host. Two classes of pathogenicity genes including basic and specialized pathogenicity genes (Ma et al., 2013), confer F. graminearum with the ability to colonize hosts and show tissue and host specificity (Maier et al., 2006; Zhang et al., 2012), but little is known about the regulation of tissue and host specificity. There is still a long way to go and concerted efforts will need to be made to enlighten the black box of F. graminearum–host interactions.
Acknowledgements The research in W-H.T.’s laboratory is supported by the National Basic Research Program of China (2011CB100702). Lei-Jie Jia and Wei-Hua Tang* National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China (*Author for correspondence: tel +86 21 54924072; email [email protected])
Ó 2015 The Authors New Phytologist Ó 2015 New Phytologist Trust
Forum 3
References Cohen P. 2000. The regulation of protein function by multisite phosphorylation – a 25 year update. Trends in Biochemical Sciences 25: 596–601. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819–823. Cuomo CA, G€ uldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M et al. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400–1402. Ma LJ, Geiser DM, Proctor RH, Rooney AP, O’Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K. 2013. Fusarium pathogenomics. Annual Review of Microbiology 67: 399–416. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367–373. Maier FJ, Miedaner T, Hadeler B, Felk A, Salomon S, Lemmens M, Kassner H, Schafer W. 2006. Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase (Tri5) gene in three field isolates of different chemotype and virulence. Molecular Plant Pathology 7: 449–461. Rocha O, Ansari K, Doohan FM. 2005. Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Additives & Contaminants 22: 369–378. Seshacharyulu P, Pandey P, Datta K, Batra SK. 2013. Phosphatase: PP2A structural importance, regulation and its aberrant expression in cancer. Cancer Letters 335: 9–18. Son H, Seo YS, Min K, Park AR, Lee J, Jin JM, Lin Y, Cao P, Hong SY, Kim EK et al. 2011. A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathogens 7: e1002310. Taylor RD, Saparno A, Blackwell B, Anoop V, Gleddie S, Tinker NA, Harris LJ. 2008. Proteomic analyses of Fusarium graminearum grown under mycotoxininducing conditions. Proteomics 8: 2256–2265. Walter S, Nicholson P, Doohan FM. 2010. Action and reaction of host and pathogen during Fusarium head blight disease. New Phytologist 185: 54–66. Wang C, Zhang S, Hou R, Zhao Z, Zheng Q, Xu Q, Zheng D, Wang G, Liu H, Gao X et al. 2011. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathogens 7: e1002460. Yu F, Gu Q, Yun Y, Yin Y, Xu J-R, Shim W-B, Ma Z. 2014. The TOR signaling pathway regulates vegetative development and virulence in Fusarium graminearum. New Phytologist 203: 219–232. Yun Y, Liu Z, Yin Y, Jiang J, Chen Y, Xu J-R, Ma Z. 2015. Functional analysis of the Fusarium graminearum phosphatome. New Phytologist 207: 119–134. Zhang XW, Jia LJ, Zhang Y, Jiang G, Li X, Zhang D, Tang WH. 2012. In planta stage-specific fungal gene profiling elucidates the molecular strategies of Fusarium graminearum growing inside wheat coleoptiles. Plant Cell 24: 5159–5176. Key words: fungal–plant interaction, Fusarium, mitogen-activated protein kinase (MAPK), omics, plant pathogen, secondary metabolism, signaling pathways.
New Phytologist (2015) 207: 1–3 www.newphytologist.com
