ICE1 demethylation drives the range expansion of a plant invader through cold tolerance divergence

Cold tolerance adaption is a crucial determinant for the establishment and expansion of invasive alien plants into new cold environments; however, its evolutionary mechanism is poorly understood. Crofton weed (Ageratina adenophora), a highly invasive alien plant, is continuously spreading across sub...

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Published in:	Molecular ecology Vol. 24; no. 4; pp. 835 - 850
Main Authors:	Xie, H. J., Li, H., Liu, D., Dai, W. M., He, J. Y., Lin, S., Duan, H., Liu, L. L., Chen, S. G., Song, X. L., Valverde, B. E., Qiang, S.
Format:	Journal Article
Language:	English
Published:	England Blackwell Publishing Ltd 01-02-2015
Subjects:	Adaptation, Physiological - genetics Ageratina - genetics Ageratina - physiology Ageratina adenophora Bacteriology CBF pathway China Cold Cold Temperature cold tolerance differentiation crofton weed (Ageratina adenophora) demethylation DNA Methylation Epigenesis, Genetic Evolution Flowers & plants gene expression Genetics, Population Introduced Species molecular evolution mechanism Molecular Sequence Data Nonnative species Plant Proteins - genetics Plant Weeds - genetics Plant Weeds - physiology Plants, Genetically Modified - physiology Transcription Factors - genetics Weeds China demethylation CBF pathway cold tolerance differentiation molecular evolution mechanism crofton weed (Ageratina adenophora) gene expression
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Summary:	Cold tolerance adaption is a crucial determinant for the establishment and expansion of invasive alien plants into new cold environments; however, its evolutionary mechanism is poorly understood. Crofton weed (Ageratina adenophora), a highly invasive alien plant, is continuously spreading across subtropical areas in China, north‐eastward from the first colonized south‐western tropical regions, through cold tolerance evolution. Close relations between the cold tolerance levels of 34 populations, represented by 147 accessions, and the latitude, extreme lowest temperature, coldest month average temperature, and invasion period have provided direct insight into its cold tolerance divergence. A comparative study of the CBF pathway, associated with the cold tolerance enhancement of cold‐susceptible CBF1‐transgenic plant, among four geographically distinct crofton weed populations revealed that the CBF pathway plays a key role in the observed cold tolerance divergence. Four epialleles of the cold response regulator ICE1 ranged from 66 to 50 methylated cytosines, representing a 4.4% to 3.3% methylation rate and significantly corresponding to the lowest to highest cold tolerance levels among these different populations. The significant negative relation between the transcription levels of the primary CBF pathway members, except for CBF2, and the methylation levels among the four populations firstly demonstrates that the demethylation‐upregulated transcription level of CBF pathway is responsible for this evolution. These facts, combined with the cold tolerance variation and methylation found among three native and two other introduced populations, indicate that the ICE1‐demethylated upregulation of cold tolerance may be the underlying evolutionary mechanism allowing crofton weed to expand northward in China.
Bibliography:	Ministry of Education of P. R. China - No. B07030 istex:A8F4D42FB08C4185C7D4B804AC732467E1D1438D National Basic Research and Development Programme of China - No. 2009CB1192 ArticleID:MEC13067 National Natural Science Foundation of China - No. 31070482 ark:/67375/WNG-63N8SJCL-T Fig. S1 Freezing injury symptoms of four distinct crofton weed populations (A) and drop percentage of Y(II) (B), ETR1 (C) and qP (D) under 4 °C for a continuous 6 days. Crofton weed populations were placed at −5 °C for 14 h at night and returned to a 25 °C growth chamber for 10 h during daytime. After treated for 4 days, the freezing injury symptoms of the four populations were recorded (A).Fig. S2 Full-length sequence of AaCBF1 (A, GenBank accession No. EF413000) AaCBF2 (B, GenBank accession No. KF804147) and AaCBF3 (C, GenBank accession No. KF804148) cDNA and its deduced amino acid sequence. The putative nuclear location sequences, expected position of conserved AP2 domain and acidic region are indicated by single line, arrow, and double underline, respectively. The oval shows the typical elements of AP2 domain and the boxed letters indicate the feature regions of AP2 in DREB.Fig. S3 Full-length sequence of AaICE1 (A, GenBank accession No. KF804150) and AaCOR29 (B, GenBank accession No. KF804149) cDNA and its deduced amino acid sequence. The red boxes indicate the bHLH structure of AaICE1 (A) and the dehydration feature structure of AaCOR29. (B), respectively.Fig. S4 Conserved regions of AaCOR6.6 (A) and AaCOR15a (B).Fig. S5 DNA flank sequences and the promoter elements of AaCBF1 (A), AaCBF3 (B) and AaICE1 (C) genes, respectively. Numbers indicate nucleotide locations that were calculated beginning with initiation codon ATG (the rectangle). The oval, single line and double line shows MYC, MYB and TATA box feature regions, respectively, the bigger rectangle represents for G-box.Fig. S6 qPCR analyses of relative expression of AaICE1 among BSG and XCS accessions. BSG-2 and XCS-2 has two more histidine at 45th amino acid compared with BSG-1 and XCS-1.Fig. S7 Schematic diagram of the effector constructs used in transgene experiments. The effector constructs contain the AaCBF1 cDNA.Fig. S8 Regeneration and phenotypes of crofton weed transgenic plants. (A) Regeneration of Agrobacterium-mediated AaCBF1 transformed crofton weed. (B) Plantlets of AaCBF1 transgenic individuals (TG-1 and TG-2) and BSG (CK). (C) Two-month old wild-type and transgenic plants grown at 25 °C with a 12/12 h photoperiod with 60 μmol/m2/s fluorescent light and 80% relative humidity.Fig. S9 Southern blot analysis of AaCBF1 of crofton weed transgenic plants. Genomic DNA (10 μg) was digested with EcoRI, BamHI and KpnI, separated by 1% (w/v) agarose gel electrophoresis and hybridized with DIG-labelled gene-specific AaCBF1 probes.Fig. S10 qPCR analysis of the relative expression of AaCBF1, AaCOR29, AaCOR15a and AaCOR6.6 of CBF1-transgenic crofton weed and BSG and HGG populations. Populations within each treatment time having the same letter do not differ at P < 0.05. Bar colour codes for populations: BSG, blue; HGG, red; TG-1, dark cyan and TG-2, cyan.Fig. S11 Variation of CBF1-transgenic crofton weed and BSG and HGG populations for their content of MDA (A), soluble sugar (B), soluble protein (C), SOD (D) and chlorophyll (E) under cold-treatment of −2 °C. Mean values (n = 3) are given for different populations. Populations within each treatment time having the same letter do not differ at P < 0.05.Table S1 Sample collection information for 34 geographically distinct crofton weed populations. Table S2 Primers for AaICE1, AaCBF and AaCOR genes DNA conserved regions, cDNAs and ORF flanking sequences amplification, AaICE1, AaCBF3 and HSP17.7 methylation determination and qPCR. Table S3 Programmes of AaICE1, AaCBs and AaCOR genes DNA conserved regions, cDNAs and ORFflanking sequences amplification, AaICE1, AaCBF3 and HSP17.7 methylation determination. Table S4 Single nucleotide polymorphisms of AaCBF1 sequences in four geographically distinct crofton weed populations. Table S5 The methylated sites of AaICE1 promoter sequences, AaCBF3 DNA and promoter sequences of crofton weed populations. Table S6 The methylated sites of AaICE1 in crofton weed populations.Data S1 Plant samples collected and the usage of the plant materials of geographically distinct populations. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	0962-1083 1365-294X
DOI:	10.1111/mec.13067