Vector-Virus Mutualism Accelerates Population Increase of an Invasive Whitefly

Abstract

The relationships between plant viruses, their herbivore vectors and host plants can be beneficial, neutral, or antagonistic, depending on the species involved. This variation in relationships may affect the process of biological invasion and the displacement of indigenous species by invaders when the invasive and indigenous organisms occur with niche overlap but differ in the interactions. The notorious invasive B biotype of the whitefly complex Bemisia tabaci entered China in the late 1990s and is now the predominant or only biotype in many regions of the country. Tobacco curly shoot virus (TbCSV) and Tomato yellow leaf curl China virus (TYLCCNV) are two whitefly-transmitted begomoviruses that have become widespread recently in south China. We compared the performance of the invasive B and indigenous ZHJ1 whitefly biotypes on healthy, TbCSV-infected and TYLCCNV-infected tobacco plants. Compared to its performance on healthy plants, the invasive B biotype increased its fecundity and longevity by 12 and 6 fold when feeding on TbCSV-infected plants, and by 18 and 7 fold when feeding on TYLCCNV-infected plants. Population density of the B biotype on TbCSV- and TYLCCNV-infected plants reached 2 and 13 times that on healthy plants respectively in 56 days. In contrast, the indigenous ZHJ1 performed similarly on healthy and virus-infected plants. Virus-infection status of the whiteflies per se of both biotypes showed limited effects on performance of vectors on cotton, a nonhost plant of the viruses. The indirect mutualism between the B biotype whitefly and these viruses via their host plants, and the apparent lack of such mutualism for the indigenous whitefly, may contribute to the ability of the B whitefly biotype to invade, the displacement of indigenous whiteflies, and the disease pandemics of the viruses associated with this vector.

βC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses

“…The results of Jiu et al (2007), Kempema et al (2007), and Zarate et al (2007) suggest that the increased aggregation of whitefly on TYLCCNV-infected plants may be due to possible suppression by the virus of specific JAresponsive plant genes that have defense function against the vector. Our results on the ability of ␤C1 to suppress expression of selective JA-responsive genes are consistent with this hypothesis.…”

“…Infections by TYLCCNV and TbCSV carrying satellite DNA␤ are not only associated with disease symptoms but also known to promote population increase of its vector, the type B invasive whitefly (Jiu et al 2007). Although the mutualism between the two gemini viruses and whitefly has been shown to be indirect via the host plants, the precise mechanism remains to be elucidated.…”

“…Several groups have reported increased aggregation of insect vectors on virus-infected plants (Maris et al 2004;Belliure et al 2005). In the case of insect vector for begomoviruses, Jiu et al (2007) showed that type B whiteflies have developed mutualistic relationships with satellite DNA␤-associated TYLCCNV and TbCSV to improve its performance on virus-infected plants. This mutualism has apparently accelerated an increase in type B whitefly population, which promoted virus spreading and the occurrence of DNA␤-associated disease complex.…”

Time - the emerging dimension of plant virus studies

“…Crops will foster viruses with particular ecological lifestyles. Crops provide vectors with a predictable succession of suitable herbaceous hosts on which they can reproduce rapidly and produce very large migrant populations, and virus infections often aid vector infestations and virus spread (Baker, 1960;Jiu et al, 2007). Thus, since the mid-Holocene, agriculture may have fostered the emergence, spread and dominance of virus taxa with particular ecologies suited to life in the continuously disturbed environments provided by humans.…”

Questions and Concepts in Plant Virus Evolution: a Historical Perspective

“…Also, viruses may affect the population dynamics of then insect vector. For instance, it has been shown that virus infection aas an influence on both the attraction of insect vectors by host plants and on thenreproductive potential (Fereres et al 1999;Jiu et al 2007). Interestingly, the effect of virus infection on aphid biology may depend on the transmission manner, nonpersistent or persistent (Eigenbrode et al 2002), Research on virus-vector interactions presently lags behind that on virus-host interactions.…”