Interaction Between Ustilaginoidea virens and Rice and Its Sustainable Control

doi:10.1016/j.rsci.2023.11.012

Abstract

Abstract:

Ustilaginoidea virens is a common rice pathogen that can easily lead to a decline in rice quality and the production of toxins pose potential risks to human health. In this review, we present a comprehensive literature review of research since the discovery of rice false smut. We provide a comprehensive and, at times, critical overview of the main results and findings from related research, and propose future research directions. Firstly, we delve into the interaction between U. virens and rice, including the regulation of transcription factors, the process of U. virens infecting rice panicles, and the plant immune response caused by rice infection. Following that, we discuss the identification and characterization of mycotoxins produced by the pathogenic fungus, as well as strategies for disease management. We emphasize the importance of comprehensive agricultural prevention and control methods for the sustainable management of U. virens. This knowledge will update our understanding of the interaction between U. virens and rice plants, offering a valuable perspective for those interested in U. virens.

Key words: rice false smut, flower-specific infection, mycotoxin, food safety, plant disease

Zhang Fengmin, Cao Zhenzhen, Zheng Xin, He Yuntao, Chen Mingxue, Lin Xiaoyan. Interaction Between Ustilaginoidea virens and Rice and Its Sustainable Control[J]. Rice Science, 2024, 31(3): 269-284.

Figures/Tables 4

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Gene	Deletion mutant	Gene function	Reference
UvSUN2	Reduced virulence	Necessary for growth, cell wall construction, and stress response	Yu et al, 2015
Uvt-1241	Reduced virulence	Important in growth and pathogenesis	Bo et al, 2016
UvPRO1	Reduced virulence	Important in mycelial growth and conidiation as well as stress response and pathogenesis	Lv et al, 2016
UvHOG1	Reduced virulence	Important in regulating stress response, mycelial growth, and possible secondary metabolism	Zheng et al, 2016
Uvt3277	Reduced virulence	Important functions related to pathogenesis	Zheng et al, 2017
Uv_1261	Increased virulence	Crucial to virulence and inhibition defense of rice flowers	Fan et al, 2019
UvAcI, UvPdeH	Reduced virulence	Important for the regulation of conidiation, stress response, virulence, and intracellular cyclic adenosine monophosphate levels	Guo et al, 2019
UvBI-1	Loss of virulence	Negative in mycelial growth and conidiation, and essential for stress tolerance, cell wall integrity, production of secondary metabolites, and pathogenicity	Xie et al, 2019
UvHox2	Reduced virulence	Regulation of chlamydial spore formation, conidiation, and pathogenicity	Yu J J et al, 2019
UvGATA	Reduced virulence	Important for fungi in pathogenicity and reactive oxygen stress tolerance	Yu M N et al, 2019
UvCom1	Reduced virulence	Affects vegetative growth and division, and the ability to stably utilize host nutrients	Chen et al, 2020a
UvPaL1	Reduced virulence	Affects mycelial growth, cell morphology, stress adaptation, and virulence	Chen et al, 2020b
UvHrip1	Reduced virulence	Inhibits the defense response induced by pathogen-associated molecular patterns in Arabidopsis seedlings and plants and promotes disease reproduction in Arabidopsis	Li S et al, 2020
UvAtg8	Reduced virulence	Essential for fungal growth, stress response, needle formation, secondary spore formation, and pathogenicity	Meng et al, 2020
UvPsr1	Reduced virulence	Essential for mycelial growth, conidiation, stress response, and pathogenicity	Xiong et al, 2020
MAT1-1-1, MAT1-1-2	Reduced virulence	Important in division, stress response, sexual development, and pathogenicity	Yong et al, 2020a
MAT1-1-3	Reduced virulence	Necessary for fruiting body and sclerotium formation, asexual development, and pathogenicity	Yong et al, 2020b
UvPmk1, UvCDc2	Loss of virulence	Important in conidia, stress response, and pathogenicity	Zhang et al, 2020
UvCap1	Reduced virulence	Important in development and pathogenicity	Cao et al, 2021
UvCCHC5	Reduced virulence	Affects stress response, vegetative growth, conidiation, and virulence	Chen et al, 2021a
UvEC1	Reduced virulence	Affects metabolism, protein localization, catalytic activity, binding, toxin biosynthesis, and splicing	Chen et al, 2021b
UvCGBP1	Reduced virulence	Regulates fungal virulence through mitogen-activated protein kinase pathway	Chen et al, 2021c
UvCBP1	Increased virulence	Manipulates plant immunity	Li et al, 2021
UvKMT6	Reduced virulence	Affects growth, division, and pathogenicity	Meng et al, 2021
UvZnFTF1	Reduced virulence	Involved in vegetative growth, conidiation, pigment biosynthesis, and pathogenicity	Song T Q et al, 2021
UvMsn2	Reduced virulence	Regulates vegetative growth, conidiation, stress response, mitochondrial morphology, and virulence	Xu et al, 2021
UvSMEK1	Reduced virulence	Regulates pathogenicity, needle formation, and spore germination	Yu J J et al, 2021
UvZC1	Reduced virulence	Involved in vegetative growth, conidium production, and rice infection, and related to the integrity of cell walls and response to oxidative stress	Yu M N et al, 2021a
UvSUN1	Reduced virulence	Essential for growth, cell wall integrity, and pathogenicity	Yu M N et al, 2021b
Uvste50	Reduced virulence	Affects the formation of conidia and rice false smut balls	Cao et al, 2022
UvCCHC4	Reduced virulence	Affects the expression of genes related to mitochondrial biogenesis, ribosomes, transporters, and ribosome biogenesis	Chen et al, 2022c
UvWhi2	Reduced virulence	Necessary for fungal growth, stress response, and secondary spore formation	Meng et al, 2022a
UvKMT2	Reduced virulence	Helpful in development, secondary spore formation, virulence, and various stress responses	Meng et al, 2022b
UvbZIP12	Reduced virulence	Involved in the regulation of growth, development, and abiotic stress tolerance, but is not necessary for pathogenicity	Qu et al, 2022a
UvbZIP6	Reduced virulence	Involved in growth, needle growth, stress response, and ball formation	Qu et al, 2022b
UvAtg14	Reduced virulence	Contributes to mycelial growth, conidiation, and pathogenicity	Yu J J et al, 2022
UvAtg7	Reduced virulence	Contributes to mycelial growth, virulence, asexual reproduction, and cell stress response	Yu J J et al, 2022
UvZnFTF2	Reduced virulence	Involved in development and pathogenicity	Song T Q et al, 2022
UvVEA	Reduced virulence	Affects the formation of chlamydia spores and the development of rice false smut balls	Yu M N et al, 2022
UvSorA, UvSorB	Reduced virulence	Important in mycelial growth, sporulation, cell wall integrity, stress response, and phytotoxicity	Zhang X P et al, 2022
UvATG6	Reduced virulence	Eliminates autophagy of U. virens and reducing growth, conidium production and germination, and virulence	Gu et al, 2023
UvATF21	Reduced virulence	Crucial in vegetative growth, meristem, stress response, and full virulence	Liu Y R et al, 2023
UvHst2	Reduced virulence	As a global regulator of secondary metabolism in U. virens	Liu L et al, 2023
UvSnf1	Reduced virulence	Plays vital roles in virulence and carbon source utilization in U. virens	Wen et al, 2023a
UvGHF1	Reduced virulence	An essential virulence factor and elicits plant immunity as a pathogen-associated molecular pattern	Zou et al, 2023
Uv1809	Increased virulence	Inhibits rice immunity and promotes U. virens infection	Chen et al, 2024

Gene	Deletion mutant	Gene function	Reference
UvSUN2	Reduced virulence	Necessary for growth, cell wall construction, and stress response	Yu et al, 2015
Uvt-1241	Reduced virulence	Important in growth and pathogenesis	Bo et al, 2016
UvPRO1	Reduced virulence	Important in mycelial growth and conidiation as well as stress response and pathogenesis	Lv et al, 2016
UvHOG1	Reduced virulence	Important in regulating stress response, mycelial growth, and possible secondary metabolism	Zheng et al, 2016
Uvt3277	Reduced virulence	Important functions related to pathogenesis	Zheng et al, 2017
Uv_1261	Increased virulence	Crucial to virulence and inhibition defense of rice flowers	Fan et al, 2019
UvAcI, UvPdeH	Reduced virulence	Important for the regulation of conidiation, stress response, virulence, and intracellular cyclic adenosine monophosphate levels	Guo et al, 2019
UvBI-1	Loss of virulence	Negative in mycelial growth and conidiation, and essential for stress tolerance, cell wall integrity, production of secondary metabolites, and pathogenicity	Xie et al, 2019
UvHox2	Reduced virulence	Regulation of chlamydial spore formation, conidiation, and pathogenicity	Yu J J et al, 2019
UvGATA	Reduced virulence	Important for fungi in pathogenicity and reactive oxygen stress tolerance	Yu M N et al, 2019
UvCom1	Reduced virulence	Affects vegetative growth and division, and the ability to stably utilize host nutrients	Chen et al, 2020a
UvPaL1	Reduced virulence	Affects mycelial growth, cell morphology, stress adaptation, and virulence	Chen et al, 2020b
UvHrip1	Reduced virulence	Inhibits the defense response induced by pathogen-associated molecular patterns in Arabidopsis seedlings and plants and promotes disease reproduction in Arabidopsis	Li S et al, 2020
UvAtg8	Reduced virulence	Essential for fungal growth, stress response, needle formation, secondary spore formation, and pathogenicity	Meng et al, 2020
UvPsr1	Reduced virulence	Essential for mycelial growth, conidiation, stress response, and pathogenicity	Xiong et al, 2020
MAT1-1-1, MAT1-1-2	Reduced virulence	Important in division, stress response, sexual development, and pathogenicity	Yong et al, 2020a
MAT1-1-3	Reduced virulence	Necessary for fruiting body and sclerotium formation, asexual development, and pathogenicity	Yong et al, 2020b
UvPmk1, UvCDc2	Loss of virulence	Important in conidia, stress response, and pathogenicity	Zhang et al, 2020
UvCap1	Reduced virulence	Important in development and pathogenicity	Cao et al, 2021
UvCCHC5	Reduced virulence	Affects stress response, vegetative growth, conidiation, and virulence	Chen et al, 2021a
UvEC1	Reduced virulence	Affects metabolism, protein localization, catalytic activity, binding, toxin biosynthesis, and splicing	Chen et al, 2021b
UvCGBP1	Reduced virulence	Regulates fungal virulence through mitogen-activated protein kinase pathway	Chen et al, 2021c
UvCBP1	Increased virulence	Manipulates plant immunity	Li et al, 2021
UvKMT6	Reduced virulence	Affects growth, division, and pathogenicity	Meng et al, 2021
UvZnFTF1	Reduced virulence	Involved in vegetative growth, conidiation, pigment biosynthesis, and pathogenicity	Song T Q et al, 2021
UvMsn2	Reduced virulence	Regulates vegetative growth, conidiation, stress response, mitochondrial morphology, and virulence	Xu et al, 2021
UvSMEK1	Reduced virulence	Regulates pathogenicity, needle formation, and spore germination	Yu J J et al, 2021
UvZC1	Reduced virulence	Involved in vegetative growth, conidium production, and rice infection, and related to the integrity of cell walls and response to oxidative stress	Yu M N et al, 2021a
UvSUN1	Reduced virulence	Essential for growth, cell wall integrity, and pathogenicity	Yu M N et al, 2021b
Uvste50	Reduced virulence	Affects the formation of conidia and rice false smut balls	Cao et al, 2022
UvCCHC4	Reduced virulence	Affects the expression of genes related to mitochondrial biogenesis, ribosomes, transporters, and ribosome biogenesis	Chen et al, 2022c
UvWhi2	Reduced virulence	Necessary for fungal growth, stress response, and secondary spore formation	Meng et al, 2022a
UvKMT2	Reduced virulence	Helpful in development, secondary spore formation, virulence, and various stress responses	Meng et al, 2022b
UvbZIP12	Reduced virulence	Involved in the regulation of growth, development, and abiotic stress tolerance, but is not necessary for pathogenicity	Qu et al, 2022a
UvbZIP6	Reduced virulence	Involved in growth, needle growth, stress response, and ball formation	Qu et al, 2022b
UvAtg14	Reduced virulence	Contributes to mycelial growth, conidiation, and pathogenicity	Yu J J et al, 2022
UvAtg7	Reduced virulence	Contributes to mycelial growth, virulence, asexual reproduction, and cell stress response	Yu J J et al, 2022
UvZnFTF2	Reduced virulence	Involved in development and pathogenicity	Song T Q et al, 2022
UvVEA	Reduced virulence	Affects the formation of chlamydia spores and the development of rice false smut balls	Yu M N et al, 2022
UvSorA, UvSorB	Reduced virulence	Important in mycelial growth, sporulation, cell wall integrity, stress response, and phytotoxicity	Zhang X P et al, 2022
UvATG6	Reduced virulence	Eliminates autophagy of U. virens and reducing growth, conidium production and germination, and virulence	Gu et al, 2023
UvATF21	Reduced virulence	Crucial in vegetative growth, meristem, stress response, and full virulence	Liu Y R et al, 2023
UvHst2	Reduced virulence	As a global regulator of secondary metabolism in U. virens	Liu L et al, 2023
UvSnf1	Reduced virulence	Plays vital roles in virulence and carbon source utilization in U. virens	Wen et al, 2023a
UvGHF1	Reduced virulence	An essential virulence factor and elicits plant immunity as a pathogen-associated molecular pattern	Zou et al, 2023
Uv1809	Increased virulence	Inhibits rice immunity and promotes U. virens infection	Chen et al, 2024

Name	Source	Antibacterial mechanism	Reference
Microbial inoculum agent
JN005	Bacillus subtilis	Inhibition of mycelial growth	Guan et al, 2016
E337	Antennariella placitae	Increase rice yield and reduce the severity of rice false smut in susceptible rice plants	Andargie et al, 2017
RSE5814	Paenibacillus polymyxa	Inhibition of mycelial growth	Liu et al, 2017
NKG-2	Bacillus velezensis	Inhibition of mycelial growth	Myo et al, 2019
Jt84	Bacillus amyloliquefaciens	Inhibition of mycelial growth	Zhang et al, 2021
BFC-33	Bacillus fluminensis	Enhance the defense response of plant seedlings	Al-Shwaiman et al, 2022
BR-01	Bacillus velezensis	Produce antimicrobial peptides	Zhou et al, 2022
Chemical agent
Azoxystrobin and Difenconazole, Metiram and Pyraclostrobin	Mixed bactericides	Reduce the incidence of disease in the field and increase yield	Muniraju et al, 2017
Ethylicin	Organosulfur compound	Inhibition of mycelial growth	Fu et al, 2018
Quicklime	CaO	Reduce the number of chlamydia spores in field soil	Ashizawa, 2019
Trifloxystrobin-Tebuconazole	Triazole group and strobilurin	Reduce disease intensity and increase yield	Duraisamy et al, 2019
Kresoxim methyl	A new broad spectrum strobilurin group of fungicide	Interfere with respiration in plant pathogenic fungi	Duraisamy et al, 2019
Propiconazole	Triazole fungicide	Demethylation inhibitor of fungal sterol biosynthesis	Duraisamy et al, 2019
Chelerythrine	Alkaloid	Broken mycelium membrane and spore reactive oxygen species accumulation	Wei et al, 2020
Osthole@guar gum	Composite material	Destroy the cell wall of U. viren	Hu et al, 2022b
Sanmate	Benzimidazole methyl carbamate	Reduce rice disease ear rate and disease index	Song J H et al, 2022a
Salicyl hydroxamic acid	Extraquinone inhibitor	Inhibition of mycelial growth, conidial germination, peroxidase, and esterase activities	Song J H et al, 2022b
Pyraclostrobin, azoxystrobin	Extraquinone inhibitor	Reduce rice disease ear rate and disease index	Song J H et al, 2022c

Name	Source	Antibacterial mechanism	Reference
Microbial inoculum agent
JN005	Bacillus subtilis	Inhibition of mycelial growth	Guan et al, 2016
E337	Antennariella placitae	Increase rice yield and reduce the severity of rice false smut in susceptible rice plants	Andargie et al, 2017
RSE5814	Paenibacillus polymyxa	Inhibition of mycelial growth	Liu et al, 2017
NKG-2	Bacillus velezensis	Inhibition of mycelial growth	Myo et al, 2019
Jt84	Bacillus amyloliquefaciens	Inhibition of mycelial growth	Zhang et al, 2021
BFC-33	Bacillus fluminensis	Enhance the defense response of plant seedlings	Al-Shwaiman et al, 2022
BR-01	Bacillus velezensis	Produce antimicrobial peptides	Zhou et al, 2022
Chemical agent
Azoxystrobin and Difenconazole, Metiram and Pyraclostrobin	Mixed bactericides	Reduce the incidence of disease in the field and increase yield	Muniraju et al, 2017
Ethylicin	Organosulfur compound	Inhibition of mycelial growth	Fu et al, 2018
Quicklime	CaO	Reduce the number of chlamydia spores in field soil	Ashizawa, 2019
Trifloxystrobin-Tebuconazole	Triazole group and strobilurin	Reduce disease intensity and increase yield	Duraisamy et al, 2019
Kresoxim methyl	A new broad spectrum strobilurin group of fungicide	Interfere with respiration in plant pathogenic fungi	Duraisamy et al, 2019
Propiconazole	Triazole fungicide	Demethylation inhibitor of fungal sterol biosynthesis	Duraisamy et al, 2019
Chelerythrine	Alkaloid	Broken mycelium membrane and spore reactive oxygen species accumulation	Wei et al, 2020
Osthole@guar gum	Composite material	Destroy the cell wall of U. viren	Hu et al, 2022b
Sanmate	Benzimidazole methyl carbamate	Reduce rice disease ear rate and disease index	Song J H et al, 2022a
Salicyl hydroxamic acid	Extraquinone inhibitor	Inhibition of mycelial growth, conidial germination, peroxidase, and esterase activities	Song J H et al, 2022b
Pyraclostrobin, azoxystrobin	Extraquinone inhibitor	Reduce rice disease ear rate and disease index	Song J H et al, 2022c