Scientia Agricultura Sinica ›› 2020, Vol. 53 ›› Issue (23): 4791-4801.doi: 10.3864/j.issn.0578-1752.2020.23.006

• PLANT PROTECTION • Previous Articles     Next Articles

The Evolutionary Dynamics and Adaptive Evolution of Tomato Chlorosis Virus

ZOU LinFeng1(),TU LiQin2,SHEN JianGuo3,DU ZhenGuo1,CAI Wei4,JI YingHua2(),GAO FangLuan1()   

  1. 1Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou 350002
    2Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014
    3Technology Center of Fuzhou Customs District, Fuzhou 350001
    4Comprehensive Technical Service Center of Rongcheng Customs District, Fuqing 350300, Fujian
  • Received:2020-07-02 Accepted:2020-07-24 Online:2020-12-01 Published:2020-12-09
  • Contact: YingHua JI,FangLuan GAO E-mail:2641144827@qq.com;jiyinghua@jaas.ac.cn;raindy@fafu.edu.cn

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Abstract:

【Objective】Tomato chlorosis virus (ToCV), a member of the genus Crinivirus in the family Closteroviridae, has emerged as one of the most prevalent viruses in tomato and other vegetable plants in China. The objectives of this study are to investigate the evolutionary history of ToCV, particularly when and where this virus was introduced into China, and to elucidate its adaptive evolutionary mechanism. 【Method】A specific primer pair flanking the coat protein gene (CP) of ToCV was designed. The CP of 13 randomly selected ToCV isolates from China was sequenced after reverse transcription and amplification using this primer pair. In addition to the novel sequence data, all published CP sequences with known sampling dates and geographic locations were obtained to assemble a total data set consisting of 103 CP sequences. A date-randomization test (DRT) was performed to assess the temporal signal in the data set and Bayesian phylodynamic framework was used to reconstruct the temporal dynamics of ToCV. Simultaneously, phylogeny-trait association analysis was used to identify whether geographic factors are involved in the adaptive evolution of ToCV. 【Result】A fragment with expected size (≈800 bp) was obtained from all the 13 ToCV-positive samples selected in this study. The CP of the 13 ToCV isolates shared more than 98% nucleotide identity with the reported sequences of other ToCV isolates. The 95% credibility intervals of rate estimate from the real sampling dates did not overlap with those from 10 replicate data sets with cluster permuted sampling date, indicating the presence of sufficient temporal signal in the sequence data allowing us to proceed with the Bayesian molecular dating analyses. Bayesian phylogenetic analyses showed that the estimated time of the most recent common ancestor of ToCV was 1920 CE (95% credibility interval 1849-1976) and the ToCV in mainland China was introduced from the USA at around 2005 CE. ToCV has been evolving at a rate of 1.12×10 -3 substitutions/site/year (95% credibility interval 6.08×10 -4-1.73×10 -3). This substitution rate is comparable to those estimated for animal RNA viruses, indicating that ToCV has been undergoing rapid evolutionary dynamics. In addition, significant association index, parsimony score and maximum monophyletic clade were observed when ToCV isolates were grouped by geographic origin (P<0.01), indicating a strong association between geographic factors and the adaptive evolution of ToCV. 【Conclusion】ToCV has been undergoing rapid evolutionary dynamics and its evolution was driven by geographic adaptation. These findings will be helpful in increasing our knowledge on the epidemiology of ToCV and have potential implications for developing more effective control strategies against this pathogen.

Key words: tomato chlorosis virus (ToCV), Bayesian phylodynamics, substitution rate, temporal signal, adaptive evolution

Table 1

ToCV isolates information used in this study"

分离物
Isolate		 国家
Country		 采样日期
Sampling date		 序列登录号
Accession number		 分离物
Isolate		 国家
Country		 采样日期
Sampling date		 序列登录号
Accession number
BR: Taquara:15 巴西Brazil 2015 KY569401 Gr-535 希腊Greece 2008 EU284744
ToC-Br2 巴西Brazil 2006 JQ952601 To-Il1970 希腊Greece 2011 HG380085
BJ 中国China 2012-10-26 KC311375 To-Il1857 希腊Greece 2011 HG380088
SDSG 中国China 2012-10 KC709510 To-Il2002 希腊Greece 2011 HG380089
Nanjing 中国China 2014-05-12 KJ815045 To-Il2010 希腊Greece 2011 HG380090
14HD-12 中国China 2014-09-25 KP335046 To-Rh1933 希腊Greece 2011 HG380084
15HD-8 中国China 2014-09-25 KR184675 To-Rh1835 希腊Greece 2011 HG380087
15-PG-9 中国China 2015-03-25 KT751008 To-Se2042 希腊Greece 2011 HG380086
NGXJZ 中国China 2014-08-03 KX272755 1 毛里求斯Mauritius 2007-02 FM206381
HBCZ 中国China 2014-08-03 KP217195 2 毛里求斯Mauritius 2007-02 FM206382
HBHS 中国China 2014-08-03 KP217196 BK2-2 韩国South Korea 2017-06-27 MG001345
HBLF 中国China 2014-08-03 KP217199 BS-4 韩国South Korea 2017-06-27 MG001346
HBSJZ 中国China 2014-08-03 KP217200 N-2 韩国South Korea 2017-06-17 MG001347
HNAYHX 中国China 2014-08-04 KP264983 JN2 韩国South Korea 2013 MG813910
HNZZZM1 中国China 2014-08-04 KP264984 NS 韩国South Korea 2013 MG813911
HNZZZM2 中国China 2014-08-04 KP264985 IS17 韩国South Korea 2013 KP114525
JLCC 中国China 2015-08-15 KU306111 YG 韩国South Korea 2013 KP114528
LNDL 中国China 2015-08-15 KU204707 IS29 韩国South Korea 2013 KP114529
LNLZ 中国China 2016-10-18 MF278016 JJ3 韩国South Korea 2013 KP114533
NMHHHT 中国China 2015-07-15 KU204709 JJ5 韩国South Korea 2013 KP114534
ToCV-YL1 中国China 2016-11-20 MF346383 JN1 韩国South Korea 2013 KP114536
SDTAFC-Bemisia tabaci 中国China 2012-10-20 KC812621 HP 韩国South Korea 2013 KP114537
Shandong 12-1 中国China 2015-11-01 KY679886 HS 韩国South Korea 2013 KP137099
Shandong 28-2 中国China 2015-11-01 KY679887 JJ 韩国South Korea 2013 KP137101
Shandong 18-3 中国China 2015-11-01 KY679888 2.5 西班牙Spain 2010 KJ200305
SDTADP 中国China 2012-10-20 KC812619 MM8 西班牙Spain 2005 KJ200307
SDTAFC 中国China 2012-10-20 KC812620 Pl-1-2 西班牙Spain 1997 KJ200309
SDLC 中国China 2012-10-20 KC812622 AT80/99-IC 西班牙Spain 2014 KJ740257
JD 中国China 2016-03-30 KX900412 AT80/99 西班牙Spain 2006 DQ136146
JD-H 中国China 2014-03-30 KX987242 XS 中国China 2011-11-19 KY618797
FQ-J 中国China 2014-03-30 KY471019 TN11 中国China 1998 MF795557
SDTAMZ 中国China 2012-10-20 KC812623 Merkez 土耳其Turkey 2015-02-03 KY419527
PD-KJ1 中国China 2015-12-15 KY206012 Kas 土耳其Turkey 2015-02-03 KY419528
PD-KJ2 中国China 2015-12-15 KY206014 AKSU8 土耳其Turkey 2012 MF576337
SDQD 中国China 2015-08-16 KT809400 ALANYA42 土耳其Turkey 2012 MF576338
SDZB 中国China 2014-08-22 KR072213 ANTALYA6 土耳其Turkey 2012 MF576339
SXJZ 中国China 2016-08-20 KX853540 ANTALYA22 土耳其Turkey 2012 MF576340
ToCV-TJ6 中国China 2014-08-07 KP219722 FETHIYE72 土耳其Turkey 2012 MF576341
ToCV-YN 中国China 2016-10-20 KY471138 FINIKE1 土耳其Turkey 2012 MF576342
BB6* 中国China 2019-03-21 MN939023 GAZIPASA4 土耳其Turkey 2012 MF576343
EB1* 中国China 2017-04-06 MN939024 KEMER20 土耳其Turkey 2012 MF576344
EB2* 中国China 2019-03-14 MN939025 KUMLUCA32 土耳其Turkey 2012 MF576345
EB6* 中国China 2019-03-14 MN939026 KUMLUCA39 土耳其Turkey 2012 MF576346
XMF3* 中国China 2017-04-12 MN939027 MANAVGAT6 土耳其Turkey 2012 MF576347
XMF4* 中国China 2017-03-30 MN939028 SERIK48 土耳其Turkey 2012 MF576348
XMF5* 中国China 2017-03-30 MN939029 TRAntToCV 土耳其Turkey 2018-03 MK248741
XMF7* 中国China 2017-04-17 MN939030 Florida 美国United States 2005 AY903448
XMF8* 中国China 2017-04-17 MN939031 Amelia 美国United States 2010-11-03 HQ879840
XS3* 中国China 2019-03-14 MN939032 FL47 美国United States 2010-11-03 HQ879841
XS5* 中国China 2019-03-14 MN939033 Tygress 美国United States 2010-11-03 HQ879842
YRDR03* 中国China 2017-04-27 MN939034 Shanty 美国United States 2010-11-03 HQ879843
YRDR12* 中国China 2017-04-27 MN939035

Fig. 1

RT-PCR amplification of CP from ToCV M：DNA分子量标准 Marker DNA (2000 bp);1—20：随机抽取的ToCV分离物PCR products of CP of ToCV randomly sampled isolates;21—23：阳性对照、阴性对照和空白对照Positive control (with known ToCV infected plant), negative control 1 (healthy plant) and negative control 2 (water), respectively"

Fig. 2

Mantel test of confounding of temporal and genetic distances The left figure shows the results for phylo-temporal cluster and the x- and y-axes on the right figure indicate differences in sampling years and genetic distance, respectively"

Fig. 3

Date-randomization test for temporal signal Real indicates the non-randomized data set, Rep 1-10 are 10 different randomizations of the dates in the data set; The 95% credibility intervals of the rate estimates from the original and the randomization data set are shown by the solid and dashed lines, respectively. The mean rate estimates from the original and the randomization data set are shown by black solid dot and hollow circles, respectively"

Table 2

Marginal likelihoods of different combinations of molecular clock model and tree prior"

分子钟模型Molecular clock model 树先验模型Tree prior 对数边际似然值Log marginal likelihood
不相关对数正态分布的宽松分子钟 Uncorrelated lognormal relaxed clock 贝叶斯天际线 Bayesian skyline -3347.81/-3347.15
不相关对数正态分布的宽松分子钟 Uncorrelated lognormal relaxed clock 恒定大小 Constant size -3348.44/-3349.36
不相关对数正态分布的宽松分子钟 Uncorrelated lognormal relaxed clock 指数增长 Exponential growth -3353.59/-3355.58
严格分子钟 Strict clock 贝叶斯天际线Bayesian skyline -3369.38/-3366.75
严格分子钟 Strict clock 恒定大小Constant size -3368.88/-3365.99
严格分子钟 Strict clock 指数增长Exponential growth -3372.35/-3371.24

Fig. 4

Phylogenetic tree inferred by Bayesian analysis of gene sequences of the CP of ToCV Posterior probability values are given at each node (only >0.95 is shown). Branch lengths are scaled in units of time, as indicated by the time axis. Branch and tip colors denote inferred location states. The root state posterior probabilities estimated for each country are shown in the inset panel on the top-left corner. Blue solid dots indicate 13 ToCV isolates sequenced in this study"

Table 3

Estimates of the substitution rate and time to the most common ancestor"

参数Parameter 数值Value
序列长度Sequence length (nt)
日期范围Date range (year) 1997-2019
样本大小Sample size 103
最近共祖时间
The most recent common ancestor (year)		 1920 (1849-1976)
替代速率
Substitution rate (subs/site/year)		 1.12×10-3 (6.08×10-4-1.73×10-3)

Table 4

Phylogeny-trait association test of the geographic structure of ToCV"

统计
Statistic		 观察平均值（95%置信区间）
Observed mean (95% CI)		 零假设平均值（95%置信区间）
Null mean (95% CI)		 P值
P-value
AI 0.20 (0.02-0.44) 8.03 (7.36-8.71) <0.001
PS 12.24 (11.00-14.00) 50.11 (48.24-51.68) <0.001
MC (巴西Brail) 1.93 (1.00-2.00) 1.00 (1.00-1.00) <0.01
MC (中国大陆Mainland China) 32.77 (20.00-50.00) 3.64 (2.80-5.60) <0.01
MC (希腊Greece) 2.87 (2.00-4.00) 1.18 (1.00-1.83) <0.01
MC (毛里求斯Mauritius) 2.00 (2.00-2.00) 1.00 (1.00-1.00) <0.01
MC (韩国South Korea) 7.00 (7.00-7.00) 1.47 (1.10-2.01) <0.01
MC (西班牙Spain) 4.17 (4.00-5.00) 1.06 (1.00-1.25) <0.01
MC (中国台湾Taiwan, China) 2.00 (2.00-2.00) 1.00 (1.00-1.00) <0.01
MC (土耳其Turkey) 10.39 (6.00-14.00) 1.49 (1.03-2.05) <0.01
MC (美国United States) 3.25 (2.00-5.00) 1.05 (1.00-1.17) <0.01
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