Feeding of Riptortus pedestris on soybean plants, the primary cause of soybean staygreen syndrome in the Huang-Huai-Hai river basin
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摘要
Staygreen syndrome or Zhengqing in soybean has recently become a major issue for Chinese growers in the Huang-Huai-Hai river basin.Although previous studies revealed that staygreen can be induced when pods/seeds are damaged, it is unknown whether virus infection or insect infestation causes staygreen.To determine whether viral infection causes staygreen, a survey of soybean staygreen incidence in the Huang-Huai-Hai river basin was conducted in 2016 and 2017.Diseased samples were collected and analyzed using DAS-ELISA for Soybean mosaic virus, Watermelon mosaic virus, Bean pod mottle virus, Cucumber mosaic virus, and Bean common mosaic virus.The survey showed that the severity of soybean staygreen syndrome was most prevalent in Beijing, Henan, Shaanxi, and some parts of Shandong provinces, with yield losses from 0 to nearly 100%, but only a small fraction of samples were positive for the tested viruses.A field cage experiment and an insecticide treatment field trial were conducted to determine the contribution of the bean bug, Riptortus pedestris, to staygreen incidence.The field cage experiment showed that R.pedestris treatment resulted in shorter plants, more empty pods, increased numbers of abnormal seeds, and decreased yields.The field experiment showed that there were fewer R.pedestris and less soybean staygreen incidence in fields treated with insecticide than in untreated control fields.Together, these results suggest that R.pedestris infestation rather than virus infection induces staygreen syndrome and that growers in this region can mitigate staygreen syndrome via bean bug control.
Staygreen syndrome or Zhengqing in soybean has recently become a major issue for Chinese growers in the Huang-Huai-Hai river basin.Although previous studies revealed that staygreen can be induced when pods/seeds are damaged, it is unknown whether virus infection or insect infestation causes staygreen.To determine whether viral infection causes staygreen, a survey of soybean staygreen incidence in the Huang-Huai-Hai river basin was conducted in 2016 and 2017.Diseased samples were collected and analyzed using DAS-ELISA for Soybean mosaic virus, Watermelon mosaic virus, Bean pod mottle virus, Cucumber mosaic virus, and Bean common mosaic virus.The survey showed that the severity of soybean staygreen syndrome was most prevalent in Beijing, Henan, Shaanxi, and some parts of Shandong provinces, with yield losses from 0 to nearly 100%, but only a small fraction of samples were positive for the tested viruses.A field cage experiment and an insecticide treatment field trial were conducted to determine the contribution of the bean bug, Riptortus pedestris, to staygreen incidence.The field cage experiment showed that R.pedestris treatment resulted in shorter plants, more empty pods, increased numbers of abnormal seeds, and decreased yields.The field experiment showed that there were fewer R.pedestris and less soybean staygreen incidence in fields treated with insecticide than in untreated control fields.Together, these results suggest that R.pedestris infestation rather than virus infection induces staygreen syndrome and that growers in this region can mitigate staygreen syndrome via bean bug control.
Staygreen syndrome or Zhengqing in soybean has recently become a major issue for Chinese growers in the Huang-Huai-Hai river basin.Although previous studies revealed that staygreen can be induced when pods/seeds are damaged, it is unknown whether virus infection or insect infestation causes staygreen.To determine whether viral infection causes staygreen, a survey of soybean staygreen incidence in the Huang-Huai-Hai river basin was conducted in 2016 and 2017.Diseased samples were collected and analyzed using DAS-ELISA for Soybean mosaic virus, Watermelon mosaic virus, Bean pod mottle virus, Cucumber mosaic virus, and Bean common mosaic virus.The survey showed that the severity of soybean staygreen syndrome was most prevalent in Beijing, Henan, Shaanxi, and some parts of Shandong provinces, with yield losses from 0 to nearly 100%, but only a small fraction of samples were positive for the tested viruses.A field cage experiment and an insecticide treatment field trial were conducted to determine the contribution of the bean bug, Riptortus pedestris, to staygreen incidence.The field cage experiment showed that R.pedestris treatment resulted in shorter plants, more empty pods, increased numbers of abnormal seeds, and decreased yields.The field experiment showed that there were fewer R.pedestris and less soybean staygreen incidence in fields treated with insecticide than in untreated control fields.Together, these results suggest that R.pedestris infestation rather than virus infection induces staygreen syndrome and that growers in this region can mitigate staygreen syndrome via bean bug control.
引文
[1]X.Z.Li,Discussions on the causes and treating measurements of Zhengqing disease of soybean,J.Hebei Agric.Sci.11(2007)64-65(in Chinese with English abstract).
[2]Y.Sakuraba,S.Y.Park,N.C.Paek,The divergent roles of staygreen(SGR)homologs in chlorophyll degradation,Mol.Cell 38(2015)390-395.
[3]C.B.Hill,G.L.Hartman,R.Esgar,H.A.Hobbs,Field evaluation of green stem disorder in soybean cultivars,Crop Sci.46(2006)879-885.
[4]H.A.Hobbs,C.B.Hill,C.R.Grau,N.C.Koval,Y.Wang,W.L.Pedersen,L.L.Domier,G.L.Hartman,Green stem disorder of soybean,Plant Dis.90(2006)513-518.
[5]V.A.Wittenbach,Effect of pod removal on leaf senescence in soybeans,Plant Physiol.70(1982)1544-1548.
[6]X.Zhang,M.Wang,T.Wu,C.Wu,B.Jiang,C.Guo,T.Han,Physiological and molecular studies of staygreen caused by pod removal and seed injury in soybean,Crop J.4(2016)435-443.
[7]D.J.Boethel,J.S.Russin,A.T.Wier,L.M.Blake,J.S.Mink,M.L.Boyd,Delayed maturity associated with southern green stink bug(Heteroptera:Pentatomidae)injury at various soybean phenological stages,J.Econ.Entomol.93(2000)707-712.
[8]T.Tsunoda,S.Moriya,Measurement of flight speed and estimation of flight distance of the bean bug,Riptortus pedestris(Fabricius)(Heteroptera:Alydidae)and the rice bug,Leptocorisa chinensis Dallas(Heteroptera:Alydidae)with a speed sensor and flight mills,Appl.Entomol.Zool.43(2008)451-456.
[9]S.Kim,U.T.Lim,New soybean variety,Agakong,as a host of Riptortus pedestris(Fabricius):study on field occurrence and biological attributes in the laboratory,J.Asia Pac.Entomol.13(2010)261-265.
[10]R.Maharjan,C.Jung,Insecticide-mediated behavioral avoidance by bean bug,Riptortus pedestris(Heteroptera:Alydidae),Entomol.Res.45(2015)184-192.
[11]B.P.Mainali,H.J.Kim,Y.N.Yoon,I.S.Oh,S.D.Bae,Evaluation of different leguminous seeds as food sources for the bean bug Riptortus pedestris,J.Asia Pac.Entomol.17(2014)115-117.
[12]S.Do Bae,H.J.Kim,B.P.Mainali,Infestation of Riptortus pedestris(Fabricius)decreases the nutritional quality and germination potential of soybean seeds,J.Asia Pac.Entomol.17(2014)477-481.
[13]S.Kim,U.T.Lim,Seasonal occurrence pattern and withinplant egg distribution of bean bug,Riptortus pedestris(Fabricius)(Hemiptera:Alydidae),and its egg parasitoids in soybean fields,Appl.Entomol.Zool.45(2010)457-464.
[14]M.M.Rahman,U.T.Lim,Evaluation of mature soybean pods as a food source for two pod-sucking bugs,Riptortus pedestris(Hemiptera:Alydidae)and Halyomorpha halys(Hemiptera:Pentatomidae),PLoS One 12(2017),e0176187.
[15]M.A.Alim,U.T.Lim,Refrigerated eggs of Riptortus pedestris(Hemiptera:Alydidae)added to aggregation pheromone traps increase field parasitism in soybean,J.Econ.Entomol.104(2011)1833-1839.
[16]H.S.Shin,T.H.Ryu,H.R.Kwon,Y.N.Youn,Aggregation pheromone secretion change of Riptortus pedestris(Hemiptera:Alydidae)depending on diet,J.Fac.Agric.Kyushu Univ.60(2015)357-362.
[17]K.Tabuchi,H.Taki,H.Iwai,N.Mizutani,K.Nagasaka,S.Moriya,R.Sasaki,Abundances of a bean bug and its natural enemy in seminatural and cultivated habitats in agricultural landscapes,Environ.Entomol.43(2014)312-319.
[18]S.Do Bae,H.J.Kim,B.P.Mainali,Changes in nutritional composition of soybean seed caused by feeding of pentatomid(Hemiptera:Pentatomidae)and alydid bugs(Hemiptera:Alydidae),J.Econ.Entomol.107(2014)1055-1060.
[19]N.Endo,K.Matsukura,T.Wada,R.Sasaki,Physiological conditions of Piezodorus hybneri(Heteroptera:Pentatomidae)attracted to synthetic pheromone of Riptortus pedestris(Heteroptera:Alydidae),Jpn.J.Appl.Entomol.Zool.50(2006)319-323.
[20]N.Endo,R.Sasaki,S.Muto,Pheromonal cross-attraction in true bugs(Heteroptera):attraction of Piezodorus hybneri(Pentatomidae)to its pheromone versus the pheromone of Riptortus pedestris(Alydidae),Environ.Entomol.39(2010)1973-1979.
[21]W.R.Fehr,C.E.Caviness,Stages of Soybean Development,Special Report 80,Cooperative Extension Service,Agriculture and Home Economic Experiment Station,Iowa State University,Ames,Iowa,USA,1977.
[22]K.Li,Q.Yang,H.Zhi,J.Gai,Identification and distribution of soybean mosaic virus strains in Southern China,Plant Dis.94(2010)351-357.
[23]K.Li,H.Zhi,Advances in resistance to soybean mosaic virus disease in soybean,Soybean Sci.35(2016)525-530.
[24]L.Gao,S.Sun,K.Li,L.Wang,W.Hou,C.Wu,H.Zhi,T.Han,Spatio-temporal characterization of changes in the resistance of widely grown soybean cultivars to Soybean mosaic virus across a century of breeding in China,Crop Past.Sci.29(2018)395-405.
[25]T.F.Han,J.Y.Gai,Phytohormonal analysis of some photoperiod effects in soybean,Acta Agron.Sin.25(1999)349-355(in Chinese with English abstract).
[26]J.K.Kim,J.B.Lee,Y.R.Huh,H.A.Jang,C.H.Kim,J.W.Yoo,B.L.Lee,Burkholderia gut symbionts enhance the innate immunity of host Riptortus pedestris,Dev.Comp.Immunol.53(2015)265-269.
[27]J.K.Kim,H.Y.Park,B.L.Lee,The symbiotic role of O-antigen of Burkholderia symbiont in association with host Riptortus pedestris,Dev.Comp.Immunol.60(2016)202-208.
[28]S.Kimura,S.Tokumaru,K.Kuge,Mode of transmission and morphological structures of two Eremothecium species between Riptortus pedestris and soybean,J.Gen.Plant Pathol.74(2008)390-394.
[29]E.Lim,J.Kim,K.S.Cho,J.G.Yun,C.G.Park,Influences of food sources on reproduction and aggregation pheromone production of Riptortus pedestris(Hemiptera:Alydidae)in its adult stage,Entomol.Res.45(2015)241-246.
[30]N.Mizutani,T.Yasuda,T.Yamacuchi,S.Moriya,Individual variation in the amounts of pheromone components in the male bean bug,Riptortus pedestris(Heteroptera:Alydidae)and its attractiveness to the same species,Appl.Entomol.Zool.42(2007)629-636.
[31]N.Endo,T.Wada,R.Sasaki,Seasonal synchrony between pheromone trap catches of the bean bug,Riptortus pedestris(Heteroptera:Alydidae)and the timing of invasion of soybean fields,Appl.Entomol.Zool.46(2011)477-482.
[32]U.T.Lim,B.P.Mainali,Effect of aggregation pheromone trap of Riptortus pedestris(Hemiptera:Alydidae)on the distribution and composition of its egg parasitoids,J.Econ.Entomol.106(2013)1973-1978.
[33]B.P.Mainali,U.T.Lim,Reproduction and dispersal pattern of egg parasitoids of Riptortus pedestris(Hemiptera:Alydidae)after installing pheromone traps plus non-viable host eggs,J.Asia Pac.Entomol.19(2016)139-143.
[34]M.M.Rahman,U.T.Lim,Females of Riptortus pedestris(Hemiptera:Alydidae)in reproductive diapause are more responsive to synthetic aggregation pheromone,J.Econ.Entomol.109(2016)2082-2089.
[35]H.Takeuchi,N.Endo,Insecticide susceptibility of Nezara viridula(Heteroptera:Pentatomidae)and three other stink bug species composing a soybean pest complex in Japan,J.Econ.Entomol.105(2012)1024-1033.
[36]T.Yamada,S.Shimada,M.Hajika,K.Hirata,K.Takahashi,T.Nagaya,H.Hamaguchi,T.Maekawa,T.Sayama,T.Hayashi,M.Ishimoto,J.Tanaka,Major QTLs associated with green stem disorder insensitivity of soybean(Glycine max(L.)Merr.),Breed.Sci.64(2014)331-338.
[37]X.Yang,P.Lundeen,M.Uphoff,Soybean varietal response and yield loss caused by Sclerotinia sclerotiorum,Plant Dis.83(1999)456-461.
[2]Y.Sakuraba,S.Y.Park,N.C.Paek,The divergent roles of staygreen(SGR)homologs in chlorophyll degradation,Mol.Cell 38(2015)390-395.
[3]C.B.Hill,G.L.Hartman,R.Esgar,H.A.Hobbs,Field evaluation of green stem disorder in soybean cultivars,Crop Sci.46(2006)879-885.
[4]H.A.Hobbs,C.B.Hill,C.R.Grau,N.C.Koval,Y.Wang,W.L.Pedersen,L.L.Domier,G.L.Hartman,Green stem disorder of soybean,Plant Dis.90(2006)513-518.
[5]V.A.Wittenbach,Effect of pod removal on leaf senescence in soybeans,Plant Physiol.70(1982)1544-1548.
[6]X.Zhang,M.Wang,T.Wu,C.Wu,B.Jiang,C.Guo,T.Han,Physiological and molecular studies of staygreen caused by pod removal and seed injury in soybean,Crop J.4(2016)435-443.
[7]D.J.Boethel,J.S.Russin,A.T.Wier,L.M.Blake,J.S.Mink,M.L.Boyd,Delayed maturity associated with southern green stink bug(Heteroptera:Pentatomidae)injury at various soybean phenological stages,J.Econ.Entomol.93(2000)707-712.
[8]T.Tsunoda,S.Moriya,Measurement of flight speed and estimation of flight distance of the bean bug,Riptortus pedestris(Fabricius)(Heteroptera:Alydidae)and the rice bug,Leptocorisa chinensis Dallas(Heteroptera:Alydidae)with a speed sensor and flight mills,Appl.Entomol.Zool.43(2008)451-456.
[9]S.Kim,U.T.Lim,New soybean variety,Agakong,as a host of Riptortus pedestris(Fabricius):study on field occurrence and biological attributes in the laboratory,J.Asia Pac.Entomol.13(2010)261-265.
[10]R.Maharjan,C.Jung,Insecticide-mediated behavioral avoidance by bean bug,Riptortus pedestris(Heteroptera:Alydidae),Entomol.Res.45(2015)184-192.
[11]B.P.Mainali,H.J.Kim,Y.N.Yoon,I.S.Oh,S.D.Bae,Evaluation of different leguminous seeds as food sources for the bean bug Riptortus pedestris,J.Asia Pac.Entomol.17(2014)115-117.
[12]S.Do Bae,H.J.Kim,B.P.Mainali,Infestation of Riptortus pedestris(Fabricius)decreases the nutritional quality and germination potential of soybean seeds,J.Asia Pac.Entomol.17(2014)477-481.
[13]S.Kim,U.T.Lim,Seasonal occurrence pattern and withinplant egg distribution of bean bug,Riptortus pedestris(Fabricius)(Hemiptera:Alydidae),and its egg parasitoids in soybean fields,Appl.Entomol.Zool.45(2010)457-464.
[14]M.M.Rahman,U.T.Lim,Evaluation of mature soybean pods as a food source for two pod-sucking bugs,Riptortus pedestris(Hemiptera:Alydidae)and Halyomorpha halys(Hemiptera:Pentatomidae),PLoS One 12(2017),e0176187.
[15]M.A.Alim,U.T.Lim,Refrigerated eggs of Riptortus pedestris(Hemiptera:Alydidae)added to aggregation pheromone traps increase field parasitism in soybean,J.Econ.Entomol.104(2011)1833-1839.
[16]H.S.Shin,T.H.Ryu,H.R.Kwon,Y.N.Youn,Aggregation pheromone secretion change of Riptortus pedestris(Hemiptera:Alydidae)depending on diet,J.Fac.Agric.Kyushu Univ.60(2015)357-362.
[17]K.Tabuchi,H.Taki,H.Iwai,N.Mizutani,K.Nagasaka,S.Moriya,R.Sasaki,Abundances of a bean bug and its natural enemy in seminatural and cultivated habitats in agricultural landscapes,Environ.Entomol.43(2014)312-319.
[18]S.Do Bae,H.J.Kim,B.P.Mainali,Changes in nutritional composition of soybean seed caused by feeding of pentatomid(Hemiptera:Pentatomidae)and alydid bugs(Hemiptera:Alydidae),J.Econ.Entomol.107(2014)1055-1060.
[19]N.Endo,K.Matsukura,T.Wada,R.Sasaki,Physiological conditions of Piezodorus hybneri(Heteroptera:Pentatomidae)attracted to synthetic pheromone of Riptortus pedestris(Heteroptera:Alydidae),Jpn.J.Appl.Entomol.Zool.50(2006)319-323.
[20]N.Endo,R.Sasaki,S.Muto,Pheromonal cross-attraction in true bugs(Heteroptera):attraction of Piezodorus hybneri(Pentatomidae)to its pheromone versus the pheromone of Riptortus pedestris(Alydidae),Environ.Entomol.39(2010)1973-1979.
[21]W.R.Fehr,C.E.Caviness,Stages of Soybean Development,Special Report 80,Cooperative Extension Service,Agriculture and Home Economic Experiment Station,Iowa State University,Ames,Iowa,USA,1977.
[22]K.Li,Q.Yang,H.Zhi,J.Gai,Identification and distribution of soybean mosaic virus strains in Southern China,Plant Dis.94(2010)351-357.
[23]K.Li,H.Zhi,Advances in resistance to soybean mosaic virus disease in soybean,Soybean Sci.35(2016)525-530.
[24]L.Gao,S.Sun,K.Li,L.Wang,W.Hou,C.Wu,H.Zhi,T.Han,Spatio-temporal characterization of changes in the resistance of widely grown soybean cultivars to Soybean mosaic virus across a century of breeding in China,Crop Past.Sci.29(2018)395-405.
[25]T.F.Han,J.Y.Gai,Phytohormonal analysis of some photoperiod effects in soybean,Acta Agron.Sin.25(1999)349-355(in Chinese with English abstract).
[26]J.K.Kim,J.B.Lee,Y.R.Huh,H.A.Jang,C.H.Kim,J.W.Yoo,B.L.Lee,Burkholderia gut symbionts enhance the innate immunity of host Riptortus pedestris,Dev.Comp.Immunol.53(2015)265-269.
[27]J.K.Kim,H.Y.Park,B.L.Lee,The symbiotic role of O-antigen of Burkholderia symbiont in association with host Riptortus pedestris,Dev.Comp.Immunol.60(2016)202-208.
[28]S.Kimura,S.Tokumaru,K.Kuge,Mode of transmission and morphological structures of two Eremothecium species between Riptortus pedestris and soybean,J.Gen.Plant Pathol.74(2008)390-394.
[29]E.Lim,J.Kim,K.S.Cho,J.G.Yun,C.G.Park,Influences of food sources on reproduction and aggregation pheromone production of Riptortus pedestris(Hemiptera:Alydidae)in its adult stage,Entomol.Res.45(2015)241-246.
[30]N.Mizutani,T.Yasuda,T.Yamacuchi,S.Moriya,Individual variation in the amounts of pheromone components in the male bean bug,Riptortus pedestris(Heteroptera:Alydidae)and its attractiveness to the same species,Appl.Entomol.Zool.42(2007)629-636.
[31]N.Endo,T.Wada,R.Sasaki,Seasonal synchrony between pheromone trap catches of the bean bug,Riptortus pedestris(Heteroptera:Alydidae)and the timing of invasion of soybean fields,Appl.Entomol.Zool.46(2011)477-482.
[32]U.T.Lim,B.P.Mainali,Effect of aggregation pheromone trap of Riptortus pedestris(Hemiptera:Alydidae)on the distribution and composition of its egg parasitoids,J.Econ.Entomol.106(2013)1973-1978.
[33]B.P.Mainali,U.T.Lim,Reproduction and dispersal pattern of egg parasitoids of Riptortus pedestris(Hemiptera:Alydidae)after installing pheromone traps plus non-viable host eggs,J.Asia Pac.Entomol.19(2016)139-143.
[34]M.M.Rahman,U.T.Lim,Females of Riptortus pedestris(Hemiptera:Alydidae)in reproductive diapause are more responsive to synthetic aggregation pheromone,J.Econ.Entomol.109(2016)2082-2089.
[35]H.Takeuchi,N.Endo,Insecticide susceptibility of Nezara viridula(Heteroptera:Pentatomidae)and three other stink bug species composing a soybean pest complex in Japan,J.Econ.Entomol.105(2012)1024-1033.
[36]T.Yamada,S.Shimada,M.Hajika,K.Hirata,K.Takahashi,T.Nagaya,H.Hamaguchi,T.Maekawa,T.Sayama,T.Hayashi,M.Ishimoto,J.Tanaka,Major QTLs associated with green stem disorder insensitivity of soybean(Glycine max(L.)Merr.),Breed.Sci.64(2014)331-338.
[37]X.Yang,P.Lundeen,M.Uphoff,Soybean varietal response and yield loss caused by Sclerotinia sclerotiorum,Plant Dis.83(1999)456-461.