Effect of a Field-Source Mixture of Citrus Viroids on the Performance of ‘Nules’ Clementine and ‘Navelina’ Sweet Orange Trees Grafted on Carrizo Citrange

Abstract

A field-source mixture of citrus viroids was characterized and shown to contain Citrus exocortis viroid (CEVd), Hop stunt viroid (HSVd), Citrus bent leaf viroid (CBLVd), and Citrus dwarfing viroid (CDVd). Sequencing results showed that: (i) CEVd contained the PL and PR characteristic of class A variants; (ii) HSVd was a noncachexia variant; (iii) CBLVd was related to CVd-Ia variants; (iv) CDVd was a mixture of two types (CVd-IIIa and CVd-IIIb) of variants. The presence of the same type of variants in inoculated clementine (Citrus clementina ‘Nules’) and sweet orange (C. sinensis ‘Navelina’) trees on Carrizo citrange (Poncirus trifoliata × C. sinensis) rootstocks was confirmed. The effect of infection was determined by assessing the performance of infected and noninfected trees growing in the field. Infection resulted in small trees with reduced canopy, yielding a reduced crop. Fruit characteristics were also affected: (i) clementine and sweet orange fruits from infected trees were larger than those from noninfected trees; (ii) clementine fruits from infected trees differed in shape from those of noninfected trees; (iii) sweet orange fruits from infected trees had maturity indexes and juice contents higher than those from noninfected trees; (iv) in both species, the density of the juice, the amount of soluble solids, and the acidity of the fruits from infected trees were lower than those of fruits from noninfected trees. Infected trees had a poorly developed root system with fibrous roots containing fewer amyloplasts than noninfected trees. The results of an in vitro assay on the induction and development of roots in cultured explants are discussed.

Microarray analysis of Etrog citron (Citrus medica L.) reveals changes in chloroplast, cell wall, peroxidase and symporter activities in response to viroid infection

“…In the case of viroid–host interactions, only limited information is available, but long‐term studies performed with citrus trees revealed that viroid‐infected trees presented a smaller root–shoot system. These plants presented only a small number of parenchyma cells containing stored carbohydrates relative to noninfected control plants (Bani Hashemian et al ., 2009). This effect is caused by a reduced source–sink transport, resulting in an unbalanced root–canopy system and, consequently, in the dwarfing associated with viroid infection.…”

“…The relation of auxin to viroid infection was reported by Duran‐Vila and Semancik (1981), who showed the inability of tomato tissue infected with CEVd to respond to exogenous auxins. This inability might be involved in the development of the pathogenic syndrome caused by CEVd, not only in tomato, but also in Carrizo citrange (Bani Hashemian et al ., 2009).…”

Viroids as Companions of a Professional Career

“…Symptom evaluation was complex because trees grafted on these rootstocks were more tolerant of viroid infection, and the environmental conditions (mainly temperature) did not enhance symptom expression (Figure 4). By pulling out the trees, we were able to see/evaluate mild symptoms as well as the effect of viroid infection on the root size and therefore canopy size [41,42]. Such results were also confirmed by evaluating the performance of viroid infected trees in commercial plantations [43].…”

A Simulation of the Use of High Throughput Sequencing as Pre-Screening Assay to Enhance the Surveillance of Citrus Viruses and Viroids in the EPPO Region

“…For non-EU CTV isolates, in the EPPO A2 List, which are responsible for field stem pitting (SP) on sweet orange regardless of rootstock, and resistance-breaking (RB) of trifoliate orange and its hybrids [10], EU member states are required to plan annual surveys using a statistically sound and risk-based approach, in line with current international standards [4]. CBCVd, the smallest of the citrus viroids, a chimeric recombinant viroid between citrus exocortis viroid (CEVd) and hop stunt viroid (HSVd) [11], induces severe symptoms on trifoliate orange and Carrizo citrange [12,13].…”