title: Vector and nonvector insect feeding reduces subsequent plant susceptibility to virus transmission.
abstract: The interactions of vector-virus-plant have important ecological and evolutionary implications. While the tripartite interactions have received some attention, little is known about whether vector infestation affects subsequent viral transmission and infection. Working with the whitefly Bemisia tabaci, begomovirus and tobacco/tomato, we demonstrate that pre-infestation of plants by the whitefly vector reduced subsequent plant susceptibility to viral transmission. Pre-infestation by the cotton bollworm, a nonvector of the virus, likewise repressed subsequent viral transmission. The two types of insects, with piercing and chewing mouthparts, respectively, activated different plant signaling pathways in the interactions. Whitefly pre-infestation activated the salicylic acid (SA) signaling pathway, leading to deposition of callose that inhibited begomovirus replication/movement. Although cotton bollworm infestation elicited the jasmonic acid (JA) defense pathway and was beneficial to virus replication, the pre-infested plants repelled whiteflies from feeding and so decreased virus transmission. Experiments using a pharmaceutical approach with plant hormones or a genetic approach using hormone transgenic or mutant plants further showed that SA played a negative but JA played a positive role in begomovirus infection. These novel findings indicate that both vector and nonvector insect feeding of a plant may have substantial negative consequences for ensuing viral transmission and infection.
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, 310058, China.
authors.forename: Ping
authors.initials: P
authors.lastname: Li
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, 310058, China.
authors.forename: Yan-Ni
authors.initials: YN
authors.lastname: Shu
authors.affiliation: Institute of Biotechnology, Zhejiang University, Hangzhou, 310058, China.
authors.forename: Shuai
authors.initials: S
authors.lastname: Fu
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, 310058, China.
authors.forename: Yin-Quan
authors.initials: YQ
authors.lastname: Liu
authors.affiliation: Institute of Biotechnology, Zhejiang University, Hangzhou, 310058, China.
authors.forename: Xue-Ping
authors.initials: XP
authors.lastname: Zhou
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, 310058, China.
authors.forename: Shu-Sheng
authors.initials: SS
authors.lastname: Liu
authors.affiliation: Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou, 310058, China.
authors.forename: Xiao-Wei
authors.initials: XW
authors.lastname: Wang
mesh_terms: D000818:Animals; D053839:Begomovirus / Q000472:pathogenicity*; D003517:Cyclopentanes / Q000378:metabolism; D004198:Disease Susceptibility; D006430:Hemiptera; D060434:Herbivory; D007303:Insect Vectors / Q000472:pathogenicity* / Q000821:virology; D007915:Lepidoptera; D018551:Solanum lycopersicum / Q000502:physiology / Q000821:virology*; D009154:Mutation; D054883:Oxylipins / Q000378:metabolism; D010935:Plant Diseases / Q000821:virology*; D030821:Plants, Genetically Modified; D020156:Salicylic Acid / Q000378:metabolism; D014026:Nicotiana / Q000502:physiology / Q000821:virology*
chemical_list: D003517:Cyclopentanes; D054883:Oxylipins; C011006:jasmonic acid; D020156:Salicylic Acid
keywords: 
  Begomovirus
  ; 
  Bemisia tabaci
  ; induced plant defense; induced plant susceptibility; insect pre-infestation; insect-microbe-plant interaction; virus transmission; whitefly