Codon Usage Bias Analysis of Citrus tristeza Virus: Higher Codon Adaptation to Citrus reticulata Host.

Kajal Biswas,Prosenjit Chakraborty,Chandrika Ramadugu,Utpal Bhattacharyya,Supratik Palchoudhury,Richard Lee,Dilip Ghosh,Manjunath Keremane,Ravi Khetarpal,Palash Debnath

doi:10.3390/v11040331

Abstract

Citrus tristeza virus (CTV), a member of the aphid-transmitted closterovirus group, is the causal agent of the notorious tristeza disease in several citrus species worldwide. The codon usage patterns of viruses reflect the evolutionary changes for optimization of their survival and adaptation in their fitness to the external environment and the hosts. The codon usage adaptation of CTV to specific citrus hosts remains to be studied; thus, its role in CTV evolution is not clearly comprehended. Therefore, to better explain the host–virus interaction and evolutionary history of CTV, the codon usage patterns of the coat protein (CP) genes of 122 CTV isolates originating from three economically important citrus hosts (55 isolate from Citrus sinensis, 38 from C. reticulata, and 29 from C. aurantifolia) were studied using several codon usage indices and multivariate statistical methods. The present study shows that CTV displays low codon usage bias (CUB) and higher genomic stability. Neutrality plot and relative synonymous codon usage analyses revealed that the overall influence of natural selection was more profound than that of mutation pressure in shaping the CUB of CTV. The contribution of high-frequency codon analysis and codon adaptation index value show that CTV has host-specific codon usage patterns, resulting in higheradaptability of CTV isolates originating from C. reticulata (Cr-CTV), and low adaptability in the isolates originating from C. aurantifolia (Ca-CTV) and C. sinensis (Cs-CTV). The combination of codon analysis of CTV with citrus genealogy suggests that CTV evolved in C. reticulata or other Citrus progenitors. The outcome of the study enhances the understanding of the factors involved in viral adaptation, evolution, and fitness toward their hosts. This information will definitely help devise better management strategies of CTV.

Highlights

Citrus tristeza virus (CTV), an aphid-transmitted closterovirus, causes tristeza, a decline in citrus grafted onto CTV-susceptible rootstocks, while some isolates can cause stem pitting on sweet orange and/or grapefruit scions, resulting in reduced fruit production with poor-quality fruit
The present study indicates that (i) CTV has overall low codon usage bias (CUB), (ii) codon usage adaptations of CTV vary in different citrus hosts with higher adaptation to codon usage pattern of C. sinensis (Cs). reticulata, and (iii) codon usage adaptations have a role in the co-evolution of CTV with its host
The uneven usage of A3/U3 and G3/C3 nucleotides in AU-rich coat protein (CP) genes in the present study indicates that the compositional patterns of the CTV CP genes are more complex than the commonly observed

Summary

Introduction

Citrus tristeza virus (CTV), an aphid-transmitted closterovirus, causes tristeza, a decline in citrus grafted onto CTV-susceptible rootstocks, while some isolates can cause stem pitting on sweet orange and/or grapefruit scions, resulting in reduced fruit production with poor-quality fruit. Tristeza is the most important viral disease of citrus worldwide [1]. Tristeza destroyed over 100 million citrus trees over the last 70 years globally [2]. CTV is a phloem-limited virus having long, flexuous filamentous particles (2000 × 11 nm) consisting of a positive-sense single-stranded RNA (ssRNA) of 19.3kb in length. The ORFs 1a and b encode the replication-related proteins and are translated from the genomic RNA (gRNA), whereas ORFs 2–11 encode proteins p33, p6, p65, p61, p27 (coat protein minor; CPm), p25 (coat protein; CP), p18, p13, p20, and p23, respectively, and are expressed via 30 co-terminal sub genomic RNAs (sgRNA) [4]

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Conclusion