拟南芥及其近缘种的适应性进化研究
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摘要
植物如何适应环境变化从而生存繁衍,即适应性进化,是一个自达尔文时代起就备受关注的生物学核心科学问题.随着测序技术的快速发展,植物中各个主要类群均有物种完成了全基因组测序,并且每个物种里有许多样品完成了重测序.除了基因组外,不同维度的组学数据也得到解析,如转录组、甲基化组、小RNA组及蛋白质组等.海量的多维组学数据极大地促进了适应性进化的研究,基于多维组学数据来研究植物适应性进化的过程及机制已成为植物学研究的一个重要领域.十字花科的拟南芥是植物遗传学及分子生物学研究的模式物种,所有的研究结果及各种资源和数据使拟南芥及其近缘种也成为研究进化生物学问题的模式体系.因此,本文综述了围绕拟南芥及其近缘种近年来在植物适应性进化方面取得的重要进展,并在此基础上探讨该领域仍亟待解决的核心科学问题及未来的研究方向.
Adaptive evolution,that is,how organisms adapt to diverse habitats and reproduce efficiently,is a fundamental biological question since Darwin.With the development of genome sequencing technique,many species of diverse lineages as well as many accessions within each species have been sequenced.Besides genome sequence,more omics data sets are available now,such as transcriptome,methylome,si RNA,and proteome.High throughput genome sequencing speeds up the studies of plant adaptive evolution.Arabidopsis thaliana,the model plant from the family Brassicaceae,has many available resources or data sets,which makes A.thaliana and its closely related species become a model system to study plant adaptive evolution.Therefore,this review focuses on Arabidopsis and its relatives,to summarize the progress of plant adaptive evolution,and at the same time,to highlight the challenges to understand the mysteries of adaptive evolution.
Adaptive evolution,that is,how organisms adapt to diverse habitats and reproduce efficiently,is a fundamental biological question since Darwin.With the development of genome sequencing technique,many species of diverse lineages as well as many accessions within each species have been sequenced.Besides genome sequence,more omics data sets are available now,such as transcriptome,methylome,si RNA,and proteome.High throughput genome sequencing speeds up the studies of plant adaptive evolution.Arabidopsis thaliana,the model plant from the family Brassicaceae,has many available resources or data sets,which makes A.thaliana and its closely related species become a model system to study plant adaptive evolution.Therefore,this review focuses on Arabidopsis and its relatives,to summarize the progress of plant adaptive evolution,and at the same time,to highlight the challenges to understand the mysteries of adaptive evolution.
引文
1 Carroll S P,J?rgensen P S,Kinnison M T,et al.Applying evolutionary biology to address global challenges.Science,2014,346:1245993
2 Scheffers B R,De Meester L,Bridge T C L,et al.The broad footprint of climate change from genes to biomes to people.Science,2016,354:671-719
3 Vitti J J,Grossman S R,Sabeti P C.Detecting natural selection in genomic data.Annu Rev Genet,2013,47:97-120
4 Nielsen R.Molecular signatures of natural selection.Annu Rev Genet,2005,39:197-218
5 Wright S I,Gaut B S.Molecular population genetics and the search for adaptive evolution in plants.Mol Biol Evol,2005,22:506-519
6 Huang C H,Sun R,Hu Y,et al.Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution.Mol Biol Evol,2016,33:394-412
7 Hohmann N,Wolf E M,Lysak M A,et al.A time-calibrated road map of Brassicaceae species radiation and evolutionary history.Plant Cell,2015,27:2770-2784
8 Novikova P Y,Hohmann N,Nizhynska V,et al.Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism.Nat Genet,2016,48:1077
9 Han T S,Wu Q,Hou X H,et al.Frequent introgressions from diploid species contribute to the adaptation of the tetraploid shepherd’s purse(Capsella bursa-pastoris).Mol Plant,2015,8:427-438
10 Yant L,Bomblies K.Genomic studies of adaptive evolution in outcrossing Arabidopsis species.Curr Opin Plant Biol,2017,36:9-14
11 Knight C A,Molinari N A,Petrov D A.The large genome constraint hypothesis:evolution,ecology and phenotype.Ann Bot,2005,95:177-190
12 Gaut B S,Ross-Ibarra J.Selection on major components of angiosperm genomes.Science,2008,320:484-486
13 Ai B,Wang Z S,Ge S.Genome size is not correlated with effective population size in the Oryza species.Evolution,2012,66:3302-3310
14 Petrov D A,Sangster T A,Johnston J S,et al.Evidence for DNA loss as a determinant of genome size.Science,2000,287:1060-1062
15 Hu T T,Pattyn P,Bakker E G,et al.The Arabidopsis lyrata genome sequence and the basis of rapid genome size change.Nat Genet,2011,43:476-481
16 Guo Y L.Gene family evolution in green plants with emphasis on the origination and evolution of Arabidopsis thaliana genes.Plant J,2013,73:941-951
17 Li Z W,Chen X,Wu Q,et al.On the origin of de novo genes in Arabidopsis thaliana populations.Genome Biol Evol,2016,8:2190-2202
18 Wei L,Cao X.The effect of transposable elements on phenotypic variation:insights from plants to humans.Sci China Life Sci,2016,59:24-37
19 Chuong E B,Elde N C,Feschotte C.Regulatory activities of transposable elements:from conflicts to benefits.Nat Rev Genet,2017,18:71-86
20 Song X,Cao X.Transposon-mediated epigenetic regulation contributes to phenotypic diversity and environmental adaptation in rice.Curr Opin Plant Biol,2017,36:111-118
21 Eimer H,Sureshkumar S,Singh Yadav A,et al.RNA-dependent epigenetic silencing directs transcriptional downregulation caused by intronic repeat expansions.Cell,2018,174:1095-1105.e11
22 Cheng F,Sun C,Wu J,et al.Epigenetic regulation of subgenome dominance following whole genome triplication in Brassica rapa.New Phytol,2016,211:288-299
23 Hollister J D,Smith L M,Guo Y L,et al.Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata.Proc Natl Acad Sci USA,2011,108:2322-2327
24 Rebollo R,Romanish M T,Mager D L.Transposable elements:An abundant and natural source of regulatory sequences for host genes.Annu Rev Genet,2012,46:21-42
25 González J,Lenkov K,Lipatov M,et al.High rate of recent transposable element-induced adaptation in Drosophila melanogaster.PLo S Biol,2008,6:e251
26 González J,Karasov T L,Messer P W,et al.Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila.PLo S Genet,2010,6:e1000905
27 Li Z W,Hou X H,Chen J F,et al.Transposable elements contribute to the adaptation of Arabidopsis thaliana.Genome Biol Evol,2018,10:2140-2150
28 Guo Y L,Zhao X,Lanz C,et al.Evolution of the S-locus region in Arabidopsis relatives.Plant Physiol,2011,157:937-946
29 Chen G,Zhang B,Zhao Z,et al.“A life or death decision”for pollen tubes in S-RNase-based self-incompatibility.J Exp Bot,2010,61:2027-2037
30 Wu Q,Han T S,Chen X,et al.Long-term balancing selection contributes to adaptation in Arabidopsis and its relatives.Genome Biol,2017,18:217
31 Cao J,Schneeberger K,Ossowski S,et al.Whole-genome sequencing of multiple Arabidopsis thaliana populations.Nat Genet,2011,43:956-963
32 Horton M W,Hancock A M,Huang Y S,et al.Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the Reg Map panel.Nat Genet,2012,44:212-216
33 The 1001 Genomes Consortium.1135 genomes reveal the global pattern of polymorphism in Arabidopsis thaliana.Cell,2016,166:481-491
34 Zou Y P,Hou X H,Wu Q,et al.Adaptation of Arabidopsis thaliana to the Yangtze River basin.Genome Biol,2017,18:239
35 Long Q,Rabanal F A,Meng D,et al.Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden.Nat Genet,2013,45:884-890
36 Durvasula A,Fulgione A,Gutaker R M,et al.African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana.Proc Natl Acad Sci USA,2017,114:5213-5218
37 Zeng L,Gu Z,Xu M,et al.Discovery of a high-altitude ecotype and ancient lineage of Arabidopsis thaliana from Tibet.Sci Bull,2017,62:1628-1630
38 Becker C,Hagmann J,Müller J,et al.Spontaneous epigenetic variation in the Arabidopsis thaliana methylome.Nature,2011,480:245-249
39 Gan X,Stegle O,Behr J,et al.Multiple reference genomes and transcriptomes for Arabidopsis thaliana.Nature,2011,477:419-423
40 Schmitz R J,Schultz M D,Urich M A,et al.Patterns of population epigenomic diversity.Nature,2013,495:193-198
41 Seymour D K,Koenig D,Hagmann J,et al.Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization.PLo S Genet,2014,10:e1004785
42 Kawakatsu T,Huang S S C,Jupe F,et al.Epigenomic diversity in a global collection of Arabidopsis thaliana accessions.Cell,2016,166:492-505
43 Gaut B.Arabidopsis thaliana as a model for the genetics of local adaptation.Nat Genet,2012,44:115-116
44 Weigel D,Nordborg M.Population genomics for understanding adaptation in wild plant species.Annu Rev Genet,2015,49:315-338
45 Clark R M,Schweikert G,Toomajian C,et al.Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana.Science,2007,317:338-342
46 He F,Kang D,Ren Y,et al.Genetic diversity of the natural populations of Arabidopsis thaliana in China.Heredity,2007,99:423-431
47 Turner T L,Bourne E C,Von Wettberg E J,et al.Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils.Nat Genet,2010,42:260-263
48 Arnold B J,Lahner B,Da Costa J M,et al.Borrowed alleles and convergence in serpentine adaptation.Proc Natl Acad Sci USA,2016,113:8320-8325
49 Hancock A M,Brachi B,Faure N,et al.Adaptation to climate across the Arabidopsis thaliana genome.Science,2011,334:83-86
50 Fournier-Level A,Korte A,Cooper M D,et al.A map of local adaptation in Arabidopsis thaliana.Science,2011,334:86-89
51 Shen X,De Jonge J,Forsberg S K G,et al.Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality.PLo S Genet,2014,10:e1004842
52 Stebbins G L Jr.The significance of polyploidy in plant evolution.Am Natist,1940,74:54-66
53 Arrigo N,Barker M S.Rarely successful polyploids and their legacy in plant genomes.Curr Opin Plant Biol,2012,15:140-146
54 Weigel D.Natural variation in Arabidopsis:from molecular genetics to ecological genomics.Plant Physiol,2012,158:2-22
55 Hepworth J,Dean C.Flowering Locus C’s lessons:Conserved chromatin switches underpinning developmental timing and adaptation.Plant Physiol,2015,168:1237-1245
56 Guo Y L,Todesco M,Hagmann J,et al.Independent FLC mutations as causes of flowering-time variation in Arabidopsis thaliana and Capsella rubella.Genetics,2012,192:729-739
57 SaloméP A,Bomblies K,Laitinen R A E,et al.Genetic architecture of flowering-time variation in Arabidopsis thaliana.Genetics,2011,188:421-433
58 Leinonen P H,Remington D L,Lepp?l?J,et al.Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata.Mol Ecol,2013,22:709-723
59 Zhou C M,Zhang T Q,Wang X,et al.Molecular basis of age-dependent vernalization in Cardamine flexuosa.Science,2013,340:1097-1100
60 Lee C R,Wang B,Mojica J P,et al.Young inversion with multiple linked QTLs under selection in a hybrid zone.Nat Ecol Evol,2017,1:119
61 Xiao D,Zhao J J,Hou X L,et al.The Brassica rapa FLC homologue FLC2 is a key regulator of flowering time,identified through transcriptional co-expression networks.J Exp Bot,2013,64:4503-4516
62 Bergonzi S,Albani M C,Ver Loren van Themaat E,et al.Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina.Science,2013,340:1094-1097
63 Wang R,Farrona S,Vincent C,et al.PEP1 regulates perennial flowering in Arabis alpina.Nature,2009,459:423-427
64 Castaings L,Bergonzi S,Albani M C,et al.Evolutionary conservation of cold-induced antisense RNAs of FLOWERING LOCUS C in Arabidopsis thaliana perennial relatives.Nat Commun,2014,5:4457
65 Foxe J P,Slotte T,Stahl E A,et al.Recent speciation associated with the evolution of selfing in Capsella.Proc Natl Acad Sci USA,2009,106:5241-5245
66 Guo Y L,Bechsgaard J S,Slotte T,et al.Recent speciation of Capsella rubella from Capsella grandiflora,associated with loss of selfincompatibility and an extreme bottleneck.Proc Natl Acad Sci USA,2009,106:5246-5251
67 Hurka H,Neuffer B.Evolutionary processes in the genus Capsella(Brassicaceae).Pl Syst Evol,1997,206:295-316
68 Yang L,Wang H N,Hou X H,et al.Parallel evolution of common allelic variants confers flowering diversity in Capsella rubella.Plant Cell,2018,30:1322-1336
69 Moyers B T.Is genetic evolution predictable?Plant Cell,2018,30:1171-1172
70 Todesco M,Balasubramanian S,Hu T T,et al.Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana.Nature,2010,465:632-636
71 Kang J,Zhang H,Sun T,et al.Natural variation of C-repeat-binding factor(CBF s)genes is a major cause of divergence in freezing tolerance among a group of Arabidopsis thaliana populations along the Yangtze River in China.New Phytol,2013,199:1069-1080
72 Atwell S,Huang Y S,Vilhjálmsson B J,et al.Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines.Nature,2010,465:627-631
2 Scheffers B R,De Meester L,Bridge T C L,et al.The broad footprint of climate change from genes to biomes to people.Science,2016,354:671-719
3 Vitti J J,Grossman S R,Sabeti P C.Detecting natural selection in genomic data.Annu Rev Genet,2013,47:97-120
4 Nielsen R.Molecular signatures of natural selection.Annu Rev Genet,2005,39:197-218
5 Wright S I,Gaut B S.Molecular population genetics and the search for adaptive evolution in plants.Mol Biol Evol,2005,22:506-519
6 Huang C H,Sun R,Hu Y,et al.Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution.Mol Biol Evol,2016,33:394-412
7 Hohmann N,Wolf E M,Lysak M A,et al.A time-calibrated road map of Brassicaceae species radiation and evolutionary history.Plant Cell,2015,27:2770-2784
8 Novikova P Y,Hohmann N,Nizhynska V,et al.Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism.Nat Genet,2016,48:1077
9 Han T S,Wu Q,Hou X H,et al.Frequent introgressions from diploid species contribute to the adaptation of the tetraploid shepherd’s purse(Capsella bursa-pastoris).Mol Plant,2015,8:427-438
10 Yant L,Bomblies K.Genomic studies of adaptive evolution in outcrossing Arabidopsis species.Curr Opin Plant Biol,2017,36:9-14
11 Knight C A,Molinari N A,Petrov D A.The large genome constraint hypothesis:evolution,ecology and phenotype.Ann Bot,2005,95:177-190
12 Gaut B S,Ross-Ibarra J.Selection on major components of angiosperm genomes.Science,2008,320:484-486
13 Ai B,Wang Z S,Ge S.Genome size is not correlated with effective population size in the Oryza species.Evolution,2012,66:3302-3310
14 Petrov D A,Sangster T A,Johnston J S,et al.Evidence for DNA loss as a determinant of genome size.Science,2000,287:1060-1062
15 Hu T T,Pattyn P,Bakker E G,et al.The Arabidopsis lyrata genome sequence and the basis of rapid genome size change.Nat Genet,2011,43:476-481
16 Guo Y L.Gene family evolution in green plants with emphasis on the origination and evolution of Arabidopsis thaliana genes.Plant J,2013,73:941-951
17 Li Z W,Chen X,Wu Q,et al.On the origin of de novo genes in Arabidopsis thaliana populations.Genome Biol Evol,2016,8:2190-2202
18 Wei L,Cao X.The effect of transposable elements on phenotypic variation:insights from plants to humans.Sci China Life Sci,2016,59:24-37
19 Chuong E B,Elde N C,Feschotte C.Regulatory activities of transposable elements:from conflicts to benefits.Nat Rev Genet,2017,18:71-86
20 Song X,Cao X.Transposon-mediated epigenetic regulation contributes to phenotypic diversity and environmental adaptation in rice.Curr Opin Plant Biol,2017,36:111-118
21 Eimer H,Sureshkumar S,Singh Yadav A,et al.RNA-dependent epigenetic silencing directs transcriptional downregulation caused by intronic repeat expansions.Cell,2018,174:1095-1105.e11
22 Cheng F,Sun C,Wu J,et al.Epigenetic regulation of subgenome dominance following whole genome triplication in Brassica rapa.New Phytol,2016,211:288-299
23 Hollister J D,Smith L M,Guo Y L,et al.Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata.Proc Natl Acad Sci USA,2011,108:2322-2327
24 Rebollo R,Romanish M T,Mager D L.Transposable elements:An abundant and natural source of regulatory sequences for host genes.Annu Rev Genet,2012,46:21-42
25 González J,Lenkov K,Lipatov M,et al.High rate of recent transposable element-induced adaptation in Drosophila melanogaster.PLo S Biol,2008,6:e251
26 González J,Karasov T L,Messer P W,et al.Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila.PLo S Genet,2010,6:e1000905
27 Li Z W,Hou X H,Chen J F,et al.Transposable elements contribute to the adaptation of Arabidopsis thaliana.Genome Biol Evol,2018,10:2140-2150
28 Guo Y L,Zhao X,Lanz C,et al.Evolution of the S-locus region in Arabidopsis relatives.Plant Physiol,2011,157:937-946
29 Chen G,Zhang B,Zhao Z,et al.“A life or death decision”for pollen tubes in S-RNase-based self-incompatibility.J Exp Bot,2010,61:2027-2037
30 Wu Q,Han T S,Chen X,et al.Long-term balancing selection contributes to adaptation in Arabidopsis and its relatives.Genome Biol,2017,18:217
31 Cao J,Schneeberger K,Ossowski S,et al.Whole-genome sequencing of multiple Arabidopsis thaliana populations.Nat Genet,2011,43:956-963
32 Horton M W,Hancock A M,Huang Y S,et al.Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the Reg Map panel.Nat Genet,2012,44:212-216
33 The 1001 Genomes Consortium.1135 genomes reveal the global pattern of polymorphism in Arabidopsis thaliana.Cell,2016,166:481-491
34 Zou Y P,Hou X H,Wu Q,et al.Adaptation of Arabidopsis thaliana to the Yangtze River basin.Genome Biol,2017,18:239
35 Long Q,Rabanal F A,Meng D,et al.Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden.Nat Genet,2013,45:884-890
36 Durvasula A,Fulgione A,Gutaker R M,et al.African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana.Proc Natl Acad Sci USA,2017,114:5213-5218
37 Zeng L,Gu Z,Xu M,et al.Discovery of a high-altitude ecotype and ancient lineage of Arabidopsis thaliana from Tibet.Sci Bull,2017,62:1628-1630
38 Becker C,Hagmann J,Müller J,et al.Spontaneous epigenetic variation in the Arabidopsis thaliana methylome.Nature,2011,480:245-249
39 Gan X,Stegle O,Behr J,et al.Multiple reference genomes and transcriptomes for Arabidopsis thaliana.Nature,2011,477:419-423
40 Schmitz R J,Schultz M D,Urich M A,et al.Patterns of population epigenomic diversity.Nature,2013,495:193-198
41 Seymour D K,Koenig D,Hagmann J,et al.Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization.PLo S Genet,2014,10:e1004785
42 Kawakatsu T,Huang S S C,Jupe F,et al.Epigenomic diversity in a global collection of Arabidopsis thaliana accessions.Cell,2016,166:492-505
43 Gaut B.Arabidopsis thaliana as a model for the genetics of local adaptation.Nat Genet,2012,44:115-116
44 Weigel D,Nordborg M.Population genomics for understanding adaptation in wild plant species.Annu Rev Genet,2015,49:315-338
45 Clark R M,Schweikert G,Toomajian C,et al.Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana.Science,2007,317:338-342
46 He F,Kang D,Ren Y,et al.Genetic diversity of the natural populations of Arabidopsis thaliana in China.Heredity,2007,99:423-431
47 Turner T L,Bourne E C,Von Wettberg E J,et al.Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils.Nat Genet,2010,42:260-263
48 Arnold B J,Lahner B,Da Costa J M,et al.Borrowed alleles and convergence in serpentine adaptation.Proc Natl Acad Sci USA,2016,113:8320-8325
49 Hancock A M,Brachi B,Faure N,et al.Adaptation to climate across the Arabidopsis thaliana genome.Science,2011,334:83-86
50 Fournier-Level A,Korte A,Cooper M D,et al.A map of local adaptation in Arabidopsis thaliana.Science,2011,334:86-89
51 Shen X,De Jonge J,Forsberg S K G,et al.Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality.PLo S Genet,2014,10:e1004842
52 Stebbins G L Jr.The significance of polyploidy in plant evolution.Am Natist,1940,74:54-66
53 Arrigo N,Barker M S.Rarely successful polyploids and their legacy in plant genomes.Curr Opin Plant Biol,2012,15:140-146
54 Weigel D.Natural variation in Arabidopsis:from molecular genetics to ecological genomics.Plant Physiol,2012,158:2-22
55 Hepworth J,Dean C.Flowering Locus C’s lessons:Conserved chromatin switches underpinning developmental timing and adaptation.Plant Physiol,2015,168:1237-1245
56 Guo Y L,Todesco M,Hagmann J,et al.Independent FLC mutations as causes of flowering-time variation in Arabidopsis thaliana and Capsella rubella.Genetics,2012,192:729-739
57 SaloméP A,Bomblies K,Laitinen R A E,et al.Genetic architecture of flowering-time variation in Arabidopsis thaliana.Genetics,2011,188:421-433
58 Leinonen P H,Remington D L,Lepp?l?J,et al.Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata.Mol Ecol,2013,22:709-723
59 Zhou C M,Zhang T Q,Wang X,et al.Molecular basis of age-dependent vernalization in Cardamine flexuosa.Science,2013,340:1097-1100
60 Lee C R,Wang B,Mojica J P,et al.Young inversion with multiple linked QTLs under selection in a hybrid zone.Nat Ecol Evol,2017,1:119
61 Xiao D,Zhao J J,Hou X L,et al.The Brassica rapa FLC homologue FLC2 is a key regulator of flowering time,identified through transcriptional co-expression networks.J Exp Bot,2013,64:4503-4516
62 Bergonzi S,Albani M C,Ver Loren van Themaat E,et al.Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina.Science,2013,340:1094-1097
63 Wang R,Farrona S,Vincent C,et al.PEP1 regulates perennial flowering in Arabis alpina.Nature,2009,459:423-427
64 Castaings L,Bergonzi S,Albani M C,et al.Evolutionary conservation of cold-induced antisense RNAs of FLOWERING LOCUS C in Arabidopsis thaliana perennial relatives.Nat Commun,2014,5:4457
65 Foxe J P,Slotte T,Stahl E A,et al.Recent speciation associated with the evolution of selfing in Capsella.Proc Natl Acad Sci USA,2009,106:5241-5245
66 Guo Y L,Bechsgaard J S,Slotte T,et al.Recent speciation of Capsella rubella from Capsella grandiflora,associated with loss of selfincompatibility and an extreme bottleneck.Proc Natl Acad Sci USA,2009,106:5246-5251
67 Hurka H,Neuffer B.Evolutionary processes in the genus Capsella(Brassicaceae).Pl Syst Evol,1997,206:295-316
68 Yang L,Wang H N,Hou X H,et al.Parallel evolution of common allelic variants confers flowering diversity in Capsella rubella.Plant Cell,2018,30:1322-1336
69 Moyers B T.Is genetic evolution predictable?Plant Cell,2018,30:1171-1172
70 Todesco M,Balasubramanian S,Hu T T,et al.Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana.Nature,2010,465:632-636
71 Kang J,Zhang H,Sun T,et al.Natural variation of C-repeat-binding factor(CBF s)genes is a major cause of divergence in freezing tolerance among a group of Arabidopsis thaliana populations along the Yangtze River in China.New Phytol,2013,199:1069-1080
72 Atwell S,Huang Y S,Vilhjálmsson B J,et al.Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines.Nature,2010,465:627-631
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