Interactions Between Citrus Viroids Affect Symptom Expression and Field Performance of Clementine Trees Grafted on Trifoliate Orange

Abstract

Citrus exocortis viroid (CEVd), Citrus bent leaf viroid (CBLVd), a noncachexia variant of Hop stunt viroid (HSVd), Citrus viroid III (CVd-III), and Citrus viroid IV (CVd-IV) were co-inoculated as two-, three-, four-, and five-viroid mixtures to Clementine trees grafted on trifoliate orange to evaluate their effect on symptom expression, tree growth, and fruit yield. Most trees infected with CEVd-containing viroid mixtures developed exocortis scaling symptoms, as did CEVd alone, whereas most trees infected with HSVd- or CVd-IV-containing mixtures developed bark-cracking symptoms. Trees infected with mixtures containing both CEVd and CVd-IV revealed the existence of antagonism between these two viroids in terms of the expected bark-scaling and cracking symptoms. Synergistic interactions also were identified in trees infected with certain viroid combinations that, in spite of lacking CEVd, expressed exocortis-like scaling symptoms. Viroid interactions also affected the expected response of trees in terms of vegetative growth and fruit yield. Trees infected with viroid combinations containing CEVd or CVd-III were smaller and produced less fruit than trees infected with mixtures not containing these viroids. Viroid interactions on scion circumference and cumulative fruit yield, in terms of additivity of their effects, were statistically confirmed using a factorial analysis of variance model with two mean estimation approaches. In single-viroid infections, CEVd, CVd-III, and, to a lesser extent, CBLVd consistently and significantly reduced tree size and fruit yield. Conversely, HSVd and CVd-IV slightly increased fruit yield and reduced scion circumference. Rare and not consistent significant interactions were detected with the five-, four-, and three-viroid combinations. Antagonistic interactions between CEVd and CVd-III or CBLVd and CVd-III were revealed over the years with consistent significance. The antagonistic interaction between CEVd and CVd-IV was highly significant over the years when additional viroids were present; however, this antagonism appeared much later in the case of an exclusive interaction. HSVd and CVd-IV showed a consistent and significant synergistic interaction on yield only when both viroids were exclusively present. These results demonstrate antagonistic or synergistic relationships between citrus viroids depending on the viroid mixtures present in the host.

Estudios de Patogenicidad de Viroides del Género Apscaviroide y Hostuviroide en cítricos.

“…The host range study reported here illustrates that, like other citrus viroids, CVd-V can infect all the citrus species and cultivars tested. The phenotypic alterations incited by CVd-V infection on commercial species and cultivars are not known, but the synergistic effects described in Etrog citron co-infected with CVd-V and CBLVd or CDVd suggest that similar interactions may result in reduced tree size and yield, as reported for clementine trees grafted on trifoliate orange (Poncirus trifoliata L.) co-infected with several viroids (Vernière et al 2006). …”

“…When a plant infected with a latent or mild strain of a viroid becomes protected against subsequent infection with a severe strain of the same viroid, the typical symptoms of the second strain and its accumulation level is abolished or attenuated, a phenomenon known as "cross-protection" (Pallas and Flores, 1989;. Conversely, co-inoculation with two unrelated viroids may result in a synergistic interaction, with symptoms being more severe that those expected for purely additive effects of the two viroids (Vernière et al 2006. Given the high sequence identity between Ch5 and CVd-V, Ch5 could be regarded as a latent strain of CVd-V and a "cross-protection" phenomenon should be expected in coinfected plants.…”

Respuesta De Distintos Genotipos De Cítricos Y Géneros Afines a La Infección Con Viroides

“…The phenotypic alterations incited by CVd-V infection on commercial species and cultivars are not known, but the synergistic effects described in Etrog citron coinfected with CVd-V and CBLVd or CDVd (20) suggest that similar interactions may result in reduced tree size and yield, as reported for clementine trees grafted on trifoliate orange (Poncirus trifoliata L.) coinfected with several viroids (24).…”

DETECCIÓN Y CARACTERIZACIÓN AGRONÓMICA DE VIROIDES DE CÍTRICOS. IDENTIFICACIÓN Y CARACTERIZACIÓN MOLECULAR Y BIOLOGÍCA DE VARIANTES DEL VIROIDE DEL ENANISMO DE LOS CÍTRICOS CDVd.

“…Since bark-cracking symptoms in Tahiti lime are not infrequent in Colombia, viroid infections could be the cause ). In addition, CEVd infection of trees also co-infected with HSVd and CDVd may produce undesirable effects, such as those reported by Vernière et al, (2004Vernière et al, ( , 2006 in the case of trees grafted on the viroid-sensitive trifoliate orange. One of the viroid infected Tahiti lime sources from Magdalena municipality (Tahiti lime 6) was obtained from a tree grafted on Carrizo citrange, which is also viroid-sensitive, and therefore such trees may suffer from the sensitivity of both scion and rootstock.…”