Whitefly-begomovirus-hostplant Interactions And The Regulation Mechanism Of Hostplant In Tripartite Relationships

In recent years, MEAM1 and MED whiteflies have invaded many regions worldwide, causing destruction to the production of many crops such as cotton, tomato and cassava. The outbreak of whiteflies is always accompanied with the epidemics of begomovirus and appearance of new begomovirus species, which suggest that the interactions between whitefly and begomovirus may play a profound role in the epidemics of begomovirus and rapid spread of the whitefly. As previously showed, the interactions among whiteflies, begomoviruses and plants are complicated. The effects of virus infection on whitefly performance mediated by plant can be positive, negative or neutral depending on different combinations of whiteflies, begomoviruses and plants. Here we used two whitefly cryptic species, MEAM1 and MED; three begomoviruses, Tomato yellow leaf curl China virus (TYLCCNV), Papaya leaf curl China virus (PaLCuCNV) and Tomato yellow leaf curl virus (TYLCV) and five different hostplants, i.e. tomato Solanum lycopersicum cv. Zhongza 9, cv. CastleMart, and JA-dificient spr2 mutant plants, JA-overexpression 35S-prosystemin transgenic plants based on the wild type CastleMart along with Nicotiana benthamiana to study the impact of virus infection of host plants on whitefly performance, thus determining the combinations in which virus infection of host plants will benefit the whitefly. Besides, we explored the mechanism underlying the tripartite interactions by investigating the plant defense-related characteristics. The results are as follows:1) Comparasion of performance of MEAM1 and MED whiteflies on healthy and virus-infected tomato plantsOn S. lycopersicum cv. CastleMart or cv. Zhongza 9, TYLCCNV or TYLCV infection did not affect the performance of MEAM1 whiteflies in terms of the survival rate and fecundity. Compared to the healthy plants, the performace of MED whiteflies did not differ significantly on TYLCCNV-infected S. lycopersicum cv. CastleMart, TYLCV-infected S. lycopersicum cv. CastleMart or cv. Zhongza 9. While on tomato cv. Zhongza 9, TYLCCNV infection increased the fecundity significantly and the survival rate slightly of MED whiteflies compared to the healthy plants.2) Comparasion of performance of MEAM 1 and MED whiteflies on wild type, JA-deficient and -overexpression tomatoCompared to those on wild type tomato cv. CastleMart, the fecundity and survival rate of MEAM1 and MED whiteflies on spr2 increased significantly, while on 35S-prosystemin, the fecundity and survival rate of MEAM1 and MED whiteflies decrease significantly. These results revealed the resistant effect of tomato JA defense pathway to whiteflies. Besides, the survival rate from egg to adult of MEAM1 and MED whitefly did not differ among the three types of plants, and on 35S-prosystemin the developmental period of the two whitefly cryptic species was shortened.3) Comparasion of performance of MEAM1 and MED on healthy and virus-infected JA-deficient or overexpression tomato plantsFor the performance of MEAMl whitefly, no significant differences were found on healthy and TYLCCNV-infected spr2 or 35S-prosystemin plants. However, TYLCV infection increased the fecundity and survival rate of both MEAM 1 and MED whiteflies compared to the healthy spr2 or 35S-prosystemin, espicially on 35S-prosystemin, TYLCV infection have a significantly increase on the performance of both whiteflies.Gene expression analysis showed that in 35S-prosystemin, TYLCCNV infection down-regulated the expression levels of synthesis-related genes, regulatory factor genes and downstream defense-related genes in JA signaling pathway, and TYLCV infection down-regulated the defense-related genes but did not affect the expression of synthesis-related genes and regulatoty factor genes of JA signaling pathway.4) N. benthamiana mediated begomovirus-whitefly interactionCompared to those on healthy N. benthamiana, the survival rate of MEAM1 and MED whiteflies increased significantly when they were transferred to PaLCuCNV-or TYLCV-infected N. benthamiana plants, while the fecundity appeared no differ. However, TYLCCNV infection had no effect on the survival rate of MED whitefly.Compared with those on control cotton, the survival rates of MEAM 1 whitefly significantly decreased on the cotton with volatile from healthy, PaLCuCNV-or TYLCNNV-infected N. benthamiana. However, the survival rates were comparable between the cotton with volatile from healthy and PaLCuCNV-or TYLCNNV-infected N. benthamiana. In addition, TYLCCNV infection did not change the number of leaf trichomes, while PaLCuCNV and TYLCV infection decreased the number of trichome significantly compared to the healthy N. benthamiana.JA, SA gene expression analysis showed that compared to healthy N. benthamiana, TYLCCNV infection did not alter the expression of genes involved in JA signaling pathway, while the expression of resistance-related genes of SA signaling pathway was up-regulated and the expression of genes involved in terpenoid synthesis was down-regulated. PaLCuCNV infection did not alter the expression of genes involved in terpenoid synthesis, but up-regulated the expression of downstream resistance-related genes of SA signaling pathway.TYLCV infection did not alter the expression of genes involved in JA signaling pathway, while up-regulated the expression of downstream resistance-related genes of SA signaling pathway, and down-regulated the expression of genes involved in terpenoid synthesis.In conclusion, the interactions of whiteflies, begomoviruses and plants vary with the combinations of different species of whiteflies, begomoviruses and plants. Besides, we presumed that on hostplants of high fitness for whitefly, begomovirus infection has marginal effect on whitefly performance. At the same time, investigating the role of plant defense in the interaction of whitefly, begomovirus and plant will advance our knowledge about their complex relationships.