Phylogenetic and Molecular Variability Studies Reveal a New Genetic Clade of Citrus leprosis virus C
Abstract
:1. Introduction
2. Materials and Methods
2.1. Leprosis Surveys, Virus Detection and Isolates
2.2. Sequencing of the RNA2-Intergenic Region and p29, p15 and Partial MP Genes of CiLV-C Isolates
2.3. Phylogenetic Analysis and Estimation of Population Genetic Parameters
2.4. Estimation of Natural Selection Pressure
2.5. Recombination Analyses
2.6. Secondary Structure Prediction of P29 Proteins of Cileviruses
2.7. RT-PCR Test for Differential Detection of CiLV-C Clade-Specific Isolates
2.8. Characterization of the Isolate BR_SP_SJP_01
3. Results
3.1. CiLV-C Is the Prevalent Causal Agent of Citrus Leprosis in Brazil
3.2. Phylogenetic Analysis of the p29 and MP Genes Indicate a Second Clade within the CiLV-C Population
3.3. p15 and IR-Based Trees Suggest Recombination
3.4. Genetic Data Support the Occurrence of Two CiLV-C Clades
3.5. 5′-Proximal Region of CiLV-C RNA2 Harbors Recombination Signatures
3.6. Purifying Selection Is Acting on CiLV-C
3.7. Clade-Specific CiLV-C Isolates Can Be Differentially Detected by RT-PCR
3.8. Genomic Characterization of CiLV-C Isolate BR_SP_SJP_01
3.9. Mite-Mediated Transmission of the Isolate BR_SP_SJP_01
4. Discussion
5. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Isolate Identification 1 and Host 2 of Collection | Collection Year | Viral Genomic Region | GenBank Accession No. | Reference |
---|---|---|---|---|
Brazilian isolates | ||||
BR_MG_AFE_01 | 2012 | p29 | KR093040 | This work |
BR_SP_AMP_01 | 2012 | p29 | KR093041 | This work |
p15 | KR093078 | |||
IR | KR093139 | |||
MP | KR093106 | |||
BR_SE_AJU_01 | 2012 | p29 | KR093042 | This work |
p15 | KR093079 | |||
IR | KR093140 | |||
MP | KR093107 | |||
BR_SP_ARA_01 | 2014 | p29 | KR093043 | This work |
p15 | KR093080 | |||
IR | KR093141 | |||
MP | KR093108 | |||
BR_PA_BEL_01 | 2012 | p29 | KR093045 | This work |
p15 | KR136415 | |||
IR | KR093143 | |||
MP | KR093110 | |||
BR_SP_BRM_01 (Commelina benghalensis) | 2012 | MP | JQ944802 | [49] |
BR_SP_BRM_02 | 2012 | p29 | KR093046 | This work |
p15 | KR093084 | |||
IR | KR093144 | |||
MP | KR093112 | |||
BR_DF_BSB_01 | 2012 | p29 | KR093047 | This work |
p15 | KR093085 | |||
IR | KR093145 | |||
MP | KR093113 | |||
BR_SP_CMP_01 | 2012 | p29 | KR093049 | This work |
BR_SP_CSB_01 | 2012 | p29 | KR093050 | This work |
p15 | KR093086 | |||
BR_SP_CLN_01 | 2012 | p29 | KR093051 | This work |
p15 | KR093082 | |||
BR_MG_CGZ_01 | 2012 | p29 | KR093048 | This work |
p15 | KR093087 | |||
IR | KR093146 | |||
MP | KR093114 | |||
BR_SP_CCH_01 | 2012 | p29 | KR093052 | This work |
p15 | KR093088 | |||
IR | KR093147 | |||
MP | KR093115 | |||
BR_SP_CRD_01 | 2006 | RNA1 | DQ352194 | [32] |
RNA2 | DQ352195 | |||
BR_SP_CRD_02 | 2012 | p29 | KR093053 | This work |
p15 | KR093089 | |||
IR | KR093148 | |||
MP | KR093116 | |||
BR_SP_CRD_03 | 2012 | MP | KR093117 | This work |
BR_SP_CSM_01 | 2012 | p29 | KR093054 | This work |
p15 | KR093083 | |||
IR | KR093149 | |||
MP | KR093111 | |||
BR_GO_GYN_01 | 2012 | p29 | KR093055 | This work |
p15 | KR093090 | |||
IR | KR093150 | |||
MP | KR093118 | |||
BR_MG_LAV_01 | 2012 | MP | KR093120 | This work |
BR_SC_LSP_01 | 2012 | p29 | KR093056 | This work |
p15 | KR093091 | |||
IR | KR093151 | |||
MP | KR093119 | |||
BR_PR_LDB_01 | 2012 | p29 | KR093057 | This work |
p15 | KR093092 | |||
IR | KR093152 | |||
MP | KR093121 | |||
BR_AM_MAO_01 | 2012 | p29 | KR093058 | This work |
p15 | KR093093 | |||
IR | KR093153 | |||
MP | KR093122 | |||
BR_PR_MGF_01 | 2012 | p29 | KR093059 | This work |
p15 | KR093094 | |||
IR | KR093154 | |||
MP | KR093123 | |||
BR_SP_MRN_01 | 2012 | p29 | KR093060 | This work |
p15 | KR136416 | |||
IR | KR093155 | |||
MP | KR093124 | |||
BR_SC_NCH_01 | 2012 | p29 | KR093061 | This work |
BR_SC_NTB_01 | 2012 | p29 | KR093062 | This work |
BR_TO_PMW_01 | 2012 | p29 | KR093063 | This work |
p15 | KR093105 | |||
IR | KR093166 | |||
MP | KR093134 | |||
BR_SP_PRB_01 | 2014 | p29 | KR093064 | This work |
p15 | KR093095 | |||
IR | KR093156 | |||
MP | KR093125 | |||
BR_GO_PNT_01 | 2012 | p29 | KR093065 | This work |
p15 | KR093096 | |||
MP | KR093126 | |||
BR_SP_PRT_01 | 2012 | p29 | KR093066 | This work |
p15 | KR093097 | |||
IR | KR093157 | |||
MP | KR093127 | |||
BR_AC_RBR_01 | 2012 | p29 | KR093067 | This work |
BR_SP_ITU_01 | 2012 | p29 | KR093070 | This work |
p15 | KR093099 | |||
IR | KR093159 | |||
MP | KR093129 | |||
BR_MG_STC_01 | 2012 | p29 | KR093069 | This work |
BR_SP_SAP_01 | 2012 | p29 | KR093068 | This work |
p15 | KR093098 | |||
IR | KR093158 | |||
MP | KR093128 | |||
BR_SP_JBT_01 | 2006 | RNA1 | DQ157466 | [34] |
RNA2 | DQ157465 | |||
BR_SP_SNG_01 | 2012 | p29 | KR093071 | This work |
p15 | KR093100 | |||
IR | KR093160 | |||
MP | KR093130 | |||
BR_SP_SJP_01 | 2012 | RNA1 | KP336746 | This work |
RNA2 | KP336747 | |||
BR_SP_SJP_02 | 2012 | p29 | KR093072 | This work |
p15 | KR093101 | |||
IR | KR093161 | |||
MP | KR093135 | |||
BR_SP_SJP_03 | 2012 | p15 | KR093167 | This work |
IR | KR093162 | |||
MP | KR093136 | |||
BR_SP_SJP_04 (Commelina benghalensis) | 2013 | p29 | KR093077 | This work |
MP | KR093137 | |||
BR_SP_SDM_01 | 2015 | p29 | KT253463 | This work |
p15 | KT253469 | |||
IR | KT253475 | |||
MP | KT253481 | |||
BR_SP_SDM_02 | 2015 | p29 | KT253464 | This work |
p15 | KT253470 | |||
IR | KT253476 | |||
MP | KT253482 | |||
BR_SP_SDM_03 | 2015 | p29 | KT253465 | This work |
p15 | KT253471 | |||
IR | KT253477 | |||
MP | KT253483 | |||
BR_SP_SDM_04 | 2015 | p29 | KT253466 | This work |
p15 | KT253472 | |||
IR | KT253478 | |||
MP | KT253484 | |||
BR_SP_SDM_05 | 2015 | p29 | KT253467 | This work |
p15 | KT253473 | |||
IR | KT253479 | |||
MP | KT253485 | |||
BR_SP_SDM_06 | 2015 | p29 | KT253468 | This work |
p15 | KT253474 | |||
IR | KT253480 | |||
MP | KT253486 | |||
BR_RJ_TNG_01 | 2012 | p29 | KR093073 | This work |
p15 | KR093102 | |||
IR | KR093163 | |||
MP | KR093131 | |||
BR_SP_TTI_01 | 2012 | p29 | KR093074 | This work |
p15 | KR093103 | |||
IR | KR093164 | |||
MP | KR093132 | |||
BR_MT_TRN_01 | 2012 | p29 | KR093075 | This work |
p15 | KR093104 | |||
IR | KR093165 | |||
MP | KR093133 | |||
BR_MG_UBA_01 | 2012 | p29 | KR093076 | This work |
MP | KR093138 | |||
Isolates from other countries | ||||
AR_01 | 2012 | MP | JX163907 | [8] |
AR_02 | 2012 | p29 | KR093044 | This work |
p15 | KR093081 | |||
IR | KR093142 | |||
MP | KR093109 | |||
CO_01 | 2005 | MP | DQ272491 | [10] |
MX_01 | 2010 | MP | HQ292778 | [9] |
PA_01 | 2006 | RNA1 | DQ388512 | [50] |
RNA2 | DQ388513 | |||
PY_01 | 2012 | MP | JX163908 | [8] |
Genomic Region | Region Length (nt) | Dataset 1/# of Isolates | π | h | Hd | dS | dN | ω (dN/dS) |
---|---|---|---|---|---|---|---|---|
p29 | 792 | All/47 | 0.053 ± 0.009 | 40 | 0.990 | 0.252 ± 0.037 2 | 0.018 ± 0.003 2 | 0.07 |
CRD/38 | 0.009 ± 0.001 | 32 | 0.986 | 0.022 ± 0.004 | 0.004 ± 0.001 | 0.18 | ||
p15 | 393 | All/41 | 0.010 ± 0.001 | 30 | 0.961 | 0.014 ± 0.004 | 0.007 ± 0.002 | 0.50 |
CRD/31 | 0.010 ± 0.001 | 24 | 0.953 | 0.014 ± 0.004 | 0.008 ± 0.002 | 0.57 | ||
MP | 300 | All/46 | 0.056 ± 0.009 | 22 | 0.854 | 0.202 ± 0.043 | 0.021 ± 0.007 | 0.10 |
CRD/36 | 0.007 ± 0.001 | 17 | 0.778 | 0.019 ± 0.006 | 0.005 ± 0.002 | 0.26 | ||
IR | 940 | All/38 | 0.021 ± 0.003 | 38 | 1 | - | - | - |
CRD/28 | 0.016 ± 0.003 | 28 | 1 | - | - | - |
ORF | Nucleotide Substitution Model | Methods | Selection Pressure | Amino Acid Position in the Sequence of Isolate BR_SP_SJP_01 |
---|---|---|---|---|
p29 | TrN | SLAC-FEL-REL | purification | 27, 39, 113, 156, 157, 173, 207, 211, 227, 259 |
FEL-REL | purification | 2, 7, 23, 30, 47, 49, 57, 58, 76, 87, 99, 100, 104, 116, 118, 133, 137, 140, 151, 154, 165, 171, 172, 180, 181, 190, 196, 202, 213, 214, 217, 219, 245, 254 | ||
p15 | HKY85 | SLAC-FEL-REL | - | - |
FEL-REL | positive | 91 | ||
MP 1 | GTR | SLAC-FEL-REL | purification | 71, 112, 148 |
FEL-REL | purification | 59, 74, 80, 84, 85, 92, 93, 96, 97, 98, 99, 102, 103, 111, 115, 118, 121, 136, 146 |
BR_SP_SJP_01 | CiLV-C | CiLV-C2 Isolate Colombia | CiLV-C2 Isolate Hawaii | |||
---|---|---|---|---|---|---|
nt | aa | nt | aa | nt | aa | |
RNA1 | 85.6 | - | 60.1 | - | 60.1 | - |
ORF RdRp | 85.4 | 93.1 | 61.4 | 59.3 | 61.4 | 59.1 |
ORF p29 | 85.0 | 90.5 | 49.2 | 36.0 | 49.0 | 35.0 |
RNA2 | 88.4 | - | 52.6 | - | 52.0 | - |
ORF p15 | 99.5 | 100.0 | 44.7 | 20.8 | 45.2 | 24.6 |
ORF p61 | 81.8 | 84.0 | 52.0 | 32.0 | 51.2 | 33.1 |
ORF MP | 86.8 | 91.9 | 56.6 | 51.7 | 54.9 | 51.4 |
ORF p24 | 87.4 | 93.9 | 63.9 | 63.1 | 62.0 | 61.6 |
IR | 96.7 | - | 46.0 | - | 46.0 | - |
© 2016 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC-BY) license (http://creativecommons.org/licenses/by/4.0/).
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Ramos-González, P.L.; Chabi-Jesus, C.; Guerra-Peraza, O.; Breton, M.C.; Arena, G.D.; Nunes, M.A.; Kitajima, E.W.; Machado, M.A.; Freitas-Astúa, J. Phylogenetic and Molecular Variability Studies Reveal a New Genetic Clade of Citrus leprosis virus C. Viruses 2016, 8, 153. https://doi.org/10.3390/v8060153
Ramos-González PL, Chabi-Jesus C, Guerra-Peraza O, Breton MC, Arena GD, Nunes MA, Kitajima EW, Machado MA, Freitas-Astúa J. Phylogenetic and Molecular Variability Studies Reveal a New Genetic Clade of Citrus leprosis virus C. Viruses. 2016; 8(6):153. https://doi.org/10.3390/v8060153
Chicago/Turabian StyleRamos-González, Pedro Luis, Camila Chabi-Jesus, Orlene Guerra-Peraza, Michèle Claire Breton, Gabriella Dias Arena, Maria Andreia Nunes, Elliot Watanabe Kitajima, Marcos Antonio Machado, and Juliana Freitas-Astúa. 2016. "Phylogenetic and Molecular Variability Studies Reveal a New Genetic Clade of Citrus leprosis virus C" Viruses 8, no. 6: 153. https://doi.org/10.3390/v8060153
APA StyleRamos-González, P. L., Chabi-Jesus, C., Guerra-Peraza, O., Breton, M. C., Arena, G. D., Nunes, M. A., Kitajima, E. W., Machado, M. A., & Freitas-Astúa, J. (2016). Phylogenetic and Molecular Variability Studies Reveal a New Genetic Clade of Citrus leprosis virus C. Viruses, 8(6), 153. https://doi.org/10.3390/v8060153