Herbivore-induced activation of viral phosphatase disarms plant antiviral immunities for pathogen transmission

Abstract

22The survival of pathogens depends on their ability to overcome host immunity, 23 especially arthropod-borne viruses (arboviruses) which must withstand the immune 24 responses of both the host and the arthropod vector. Successful arboviruses often modify 25 host immunity to accelerate pathogen transmission; however, few studies have explored 26 the underlying mechanism. Here we report attracted herbivore infestation on the virus-27 infected plants promote transmission by the associated vector herbivore. This herbivore-28 induced defense suppression underpins a subversive mechanism used by Begomovirus, 29 the largest genus of plant viruses, to compromise host defense for pathogen transmission. 30 Begomovirus-infected plants accumulated βC1 proteins in the phloem where they were 31 bound to host defense regulators, transcription factor WRKY20 and two mitogen-32 activated protein kinases MPK3 and MPK6. Once perceiving whitefly herbivory or 33 endogenous secreted peptide PEP1, the plants started dephosphorylation on serine 33 and 34 stimulated βC1 protein as a phosphatase. βC1 dephosphorylated MPK3/6 and WRKY20, 35 the latter negatively regulated salicylic acid signaling and vascular callose deposition. 36This viral hijacking of WRKY20 accumulated more vascular callose by which enforced 37 whitefly prolonged salivation and phloem sap ingestion, therefore impelling more virus 38 transmission among plants. We present a scenario in which viruses dynamically respond 39 to the presence of their vectors, suppressing host immunity and promoting pathogen 40 transmission only when needed. 41 42 45 begomoviruses (Weaver et al., 2018; Gnanasekaran et al., 2019). Being obligate 46 parasites, viruses usually depend for survival on being able to spread. Only if they can 47 spread from host to host rapidly in community, viruses are then important economically.48The transmission potential of pathogens is one of the most important virulence factors 49 that cause the outbreak and epidemic of diseases, such as COVID-19 caused by SARS-50 3 associated novel coronavirus 2, SARS-CoV-2 (Li et al., 2020). Arboviruses commonly 51 modify the behavior of the arthropod vector in a manner that facilitates pathogen 52 transmission (Eigenbrode et al., 2018; Weaver et al., 2018). For instance, mosquito-53 borne bunyaviruses and flaviviruses as well as thrip-borne tospoviruses promote virus 54 transmission by directly increasing vector biting rates and by interfering with the 55 ingestion process (Stafford et al., 2011; Liu et al., 2017). Furthermore, arboviruses may 56 indirectly promote transmission by 1) manipulating the immune responses of both the 57 vector and the host, 2) suppressing host immunity by vector salivary factors, 3) 58 manipulating vector behavior, and 4) encoding transmission facilitators (Vasilakis and 59 Tesh 2015; Wang et al., 2019; Wu et al. 2019; Wu and Ye, 2020). Since plants are 60 sessile, around 80% plant viruses are transmitted by insect vectors, especially whiteflies 61 and aphids that transmit more than 50% of a...