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Rice Science ›› 2024, Vol. 31 ›› Issue (3): 269-284.DOI: 10.1016/j.rsci.2023.11.012

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  • 收稿日期:2023-09-22 接受日期:2023-11-08 出版日期:2024-05-28 发布日期:2024-06-04

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. [J]. Rice Science, 2024, 31(3): 269-284.

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链接本文: http://www.ricesci.org/CN/10.1016/j.rsci.2023.11.012

               http://www.ricesci.org/CN/Y2024/V31/I3/269

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Fig. 1. Common occurrence and field morphology of rice false smut. A, Global distribution of rice false smut. The geographical locations of rice false smut occurrence in different continents were marked with different colors. B, Occurrence of rice false smut in the field. C, Diseased rice panicles with green-black false smut balls in the paddy field.

Fig. 1. Common occurrence and field morphology of rice false smut. A, Global distribution of rice false smut. The geographical locations of rice false smut occurrence in different continents were marked with different colors. B, Occurrence of rice false smut in the field. C, Diseased rice panicles with green-black false smut balls in the paddy field.

Fig. 2. Infection cycle of Ustilaginoidea virens in the field. a, Rice false smut spores on rice panicles are transmitted to the paddy field through wind and rain. b, The overwintering sclerotia germinated to form ascospores. c, Overwintering chlamydospores germinate to form conidia. d, Ascospores produce conidia. e, Conidia are epiphytic in the roots or coleoptiles of rice seedlings. f, Conidia infect panicles at the booting stage of rice. g, Ascospores infect panicles at the booting stage of rice. h‒j, Seeds with U. virens grow in the field.

Fig. 2. Infection cycle of Ustilaginoidea virens in the field. a, Rice false smut spores on rice panicles are transmitted to the paddy field through wind and rain. b, The overwintering sclerotia germinated to form ascospores. c, Overwintering chlamydospores germinate to form conidia. d, Ascospores produce conidia. e, Conidia are epiphytic in the roots or coleoptiles of rice seedlings. f, Conidia infect panicles at the booting stage of rice. g, Ascospores infect panicles at the booting stage of rice. h‒j, Seeds with U. virens grow in the field.

Table 1. Genes controlling virulence of Ustilaginoidea virens.
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

Table 1. Genes controlling virulence of Ustilaginoidea virens.

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
Table 2. Biological and chemical agents for controlling Ustilaginoidea virens.
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

Table 2. Biological and chemical agents for controlling Ustilaginoidea virens.

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

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