Monitoring the dynamics of emergence of a non-canonical recombinant of Tomato yellow leaf curl virus and displacement of its parental viruses in tomato

Abstract

Recombinant viruses are increasingly being reported but the dynamics of their emergence is rarely documented. A new recombinant Tomato yellow leaf curl virus (TYLCV-IS76) was detected for the first time in 2010 in Southern Morocco (Souss). An original diagnostic tool was needed to fit its unusual recombination profile. Although IS76 was detected following the appearance of Tylc symptoms on tolerant tomato plants, symptoms could not be associated to IS76 or to a synergy with criniviruses. According to infection profiles of Tylc-associated viruses determined on 879 plant samples collected between 1998 and 2014 and a Bayesian inference applied to genomic sequences of representatives of TYLCV, IS76 emerged in Southern Morocco at the end of the 1990s, replaced the parental viruses between 2004 and 2012 in Souss and is spreading towards the North of Morocco. The emergence of IS76 coincides with the increasing use of tolerant cultivars in the 2000s.

Characterization of Begomoviruses Sampled during Severe Epidemics in Tomato Cultivars Carrying the Ty-1 Gene

“…In contrast, Group 2 isolates appeared related to recently discovered Moroccan isolates from the El Jadida region. Our analyses suggested that the TYLCV isolates of Group 2 are derived from a Moroccan TYLCV-IS76 recombinant through a back recombination event, as previously suggested by Belabess et al (2015) for the El Jadida isolates [ 31 ]. This scenario, with a single recombination event leading to TYLCV-IS76 and a back recombination to generate the El Jadida TYLCV type, is consistent with field observations and experimental results which suggest that TYLCV-IS76 emergence is a rare event [ 42 ].…”

“…A second phylogenetic analysis was carried out in which additional sequences from databases were included ( Figure 2 B). Interestingly, in this tree, Group 2 sequences appeared to be closely related to two Moroccan sequences (LN846613 and LN846614) ( Figure 2 B), recently described by Belabess et al (2015) [ 31 ] for isolates sampled in the El Jadida (Morocco) region; note that these are nonrecombinant isolates [ 31 ]. To rule out a potential recombinant origin for Spanish isolates in Group 2 similar to the one originating TYLCV-IS76, both an alignment with TYLCV-IS76 and TYLCSV in the recombination region ( Figure 3 ), as well as an analysis of the sequences using the RDP4 program (data not shown) were carried out; no recombination events were identified.…”

“…During recent years, we have been observing aggressive TYLCD symptoms in plants carrying the Ty-1 / Ty-3 resistance gene in tomato crops in Murcia (Southeast Spain), similar to those described in Morocco [ 31 ]. Murcia is one of the main Spanish tomato-producing areas.…”

“…We then performed a Bayesian analysis to date the diversification for TYLCV Spanish and Moroccan isolates ( Figure 5 ). We followed the same approach as in Belabess et al (2015) [ 31 ], including recombinant TYLCV-IS76 isolates and other sequences selected from the databases. The short TYLCSV derived region of TYLCV-IS76 recombinants was excluded from the alignment, and its cognate was similarly excluded from all the aligned sequences.…”

“…In this regard, a new recombinant between TYLCV and TYLCSV, called TYLCV-IS76, has been recently described in Morocco associated with Ty-1 resistant tomato plants bearing TYLCD symptoms. TYLCV-IS76-like isolates increased in frequency until the complete displacement of their parental viruses in 2012 in Morocco, coincident with the widespread use of tomato Ty-1/Ty-3 cultivars [ 31 ]. Analyses of virus accumulation under experimental conditions in resistant and susceptible tomato plants showed that TYLCV-IS76 had greater in planta fitness than its parental viruses, providing an explanation for the field observations [ 27 ].…”