MiRNA Control of Vegetative Phase Change in Trees
After germination, plants enter juvenile vegetative phase and then transition to an adult vegetative phase before producing reproductive structures. The character and timing of the juvenile-to-adult transition vary widely between species. In annual plants, this transition occurs soon after germination and usually involves relatively minor morphological changes, whereas in trees and other perennial woody plants it occurs after months or years and can involve major changes in shoot architecture. Whether this transition is controlled by the same mechanism in annual and perennial plants is unknown. In the annual forb Arabidopsis thaliana and in maize (Zea mays), vegetative phase change is controlled by the sequential activity of microRNAs miR156 and miR172. miR156 is highly abundant in seedlings and decreases during the juvenile-to-adult transition, while miR172 has an opposite expression pattern. We observed similar changes in the expression of these genes in woody species with highly differentiated, well-characterized juvenile and adult phases (Acacia confusa, Acacia colei, Eucalyptus globulus, Hedera helix, Quercus acutissima), as well as in the tree Populus x canadensis, where vegetative phase change is marked by relatively minor changes in leaf morphology and internode length. Overexpression of miR156 in transgenic P. x canadensis reduced the expression of miR156-targeted SPL genes and miR172, and it drastically prolonged the juvenile phase. Our results indicate that miR156 is an evolutionarily conserved regulator of vegetative phase change in both annual herbaceous plants and perennial trees.
Vyšlo v časopise:
MiRNA Control of Vegetative Phase Change in Trees. PLoS Genet 7(2): e32767. doi:10.1371/journal.pgen.1002012
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002012
Souhrn
After germination, plants enter juvenile vegetative phase and then transition to an adult vegetative phase before producing reproductive structures. The character and timing of the juvenile-to-adult transition vary widely between species. In annual plants, this transition occurs soon after germination and usually involves relatively minor morphological changes, whereas in trees and other perennial woody plants it occurs after months or years and can involve major changes in shoot architecture. Whether this transition is controlled by the same mechanism in annual and perennial plants is unknown. In the annual forb Arabidopsis thaliana and in maize (Zea mays), vegetative phase change is controlled by the sequential activity of microRNAs miR156 and miR172. miR156 is highly abundant in seedlings and decreases during the juvenile-to-adult transition, while miR172 has an opposite expression pattern. We observed similar changes in the expression of these genes in woody species with highly differentiated, well-characterized juvenile and adult phases (Acacia confusa, Acacia colei, Eucalyptus globulus, Hedera helix, Quercus acutissima), as well as in the tree Populus x canadensis, where vegetative phase change is marked by relatively minor changes in leaf morphology and internode length. Overexpression of miR156 in transgenic P. x canadensis reduced the expression of miR156-targeted SPL genes and miR172, and it drastically prolonged the juvenile phase. Our results indicate that miR156 is an evolutionarily conserved regulator of vegetative phase change in both annual herbaceous plants and perennial trees.
Zdroje
1. BrinkRA 1962 Phase change in higher plants and somatic cell heredity. Quart Rev Biol 37 1 22
2. DoorenbosJ 1965 Juvenile and adult phases in woody plants. Encyl Plant Physiol 15 1222 1235
3. PoethigRS 1990 Phase change and the regulation of shoot morphogenesis in plants. Science 250 923 930
4. PoethigRS 2003 Phase change and the regulation of developmental timing in plants. Science 301 334 336
5. BäurleIDeanC 2006 The timing of developmental transitions in plants. Cell 125 655 664
6. ChienJCSussexIM 1996 Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L) Heynh. Plant Physiol 111 1321 1328
7. RöbbelenG 1957 Uber Heterophyllie bei Arabidopsis thaliana (L.) Heynh. Ber Dtsch Bot Ges 70 39 44
8. TelferABollmanKMPoethigRS 1997 Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124 645 654
9. WangJWCzechBWeigelD 2009 miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138 738 749
10. WuGPoethigRS 2006 Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133 3539 3547
11. SchwabRPalatnikJFRiesterMSchommerCSchmidM 2005 Specific effects of microRNAs on the plant transcriptome. Dev Cell 8 517 527
12. GandikotaMBirkenbihlRPHohmannSCardonGHSaedlerH 2007 The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49 683 693
13. WuGParkMYConwaySRWangJWWeigelD 2009 The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138 750 759
14. YamaguchiAWuMFYangLWuGPoethigRS 2009 The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17 268 278
15. LauterNKampaniACarlsonSGoebelMMooseSP 2005 microRNA172 down-regulates Glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci USA 102 9412 9417
16. ChuckGCiganAMSaeteurnKHakeS 2007 The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39 544 549
17. SchmidMUhlenhautNHGodardFDemarMBressanR 2003 Dissection of floral induction pathways using global expression analysis. Development 130 6001 6012
18. AukermanMJSakaiH 2003 Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15 2730 2741
19. ChenX 2004 A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303 2022 2025
20. MathieuJYantLJMürdterFKüttnerFSchmidM 2009 Repression of flowering by the miR172 target SMZ. PLoS Biol 7 e1000148 doi:10.1371/journal.pbio.1000148
21. EvansMMPassasHJPoethigRS 1994 Heterochronic effects of glossy15 mutations on epidermal cell identity in maize. Development 120 1971 1981
22. PoethigRS 1988 Heterochronic mutations affecting shoot development in maize. Genetics 119 959 973
23. MooseSPSiscoPH 1994 Glossy15 controls the epidermal juvenile-to-adult phase transition in maize. Plant Cell 6 1343 1355
24. XieKWuCXiongL 2006 Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142 280 293
25. SalviSSponzaGMorganteMTomesDNiuX 2007 Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA 104 11376 11381
26. LawsonEJPoethigRS 1995 Shoot development in plants: time for a change. Trends Genet 11 263 268
27. HildebrandF 1875 Ueber die Jungendzustände solcher Pflanzen, welche im Alter vom vegetativen Charakter ihrer Verwandten abweichen. Flora 21 321 330
28. GoebelK 1889 Ueber die Jungendzustände der Pflanzen. Flora 72 1 45
29. KaplanDR 1980 Heteroblastic leaf development in Acacia. Morphological and morphogenetic implications. Cellule 73 137 203
30. JamesSABellDT 2001 Leaf morphological and anatomical characteristics of heteroblastic Eucalyptus globulus ssp globulus (Myrtaceae). Aust J Bot 49 259 269
31. WareingPFFrydmanVM 1976 General aspects of phase change, with special reference to Hedera helix L. Acta Hort 56 57 69
32. SteinOLFosketEB 1969 Comparative developmental anatomy of shoots of juvenile and adult Hedera helix. Am J Bot 56 546 551
33. ReinhartBJWeinsteinEGRhoadesMWBartelBBartelDP 2002 MicroRNAs in plants. Genes Dev 16 1616 1626
34. LuCJeongDHKulkarniKPillayMNobutaK 2008 Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci U S A 105 4951 4956
35. RajagopalanRVaucheretHTrejoJBartelDP 2006 A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20 3407 3425
36. BarakatAWallPKDiloretoSDepamphilisCWCarlsonJE 2007 Conservation and divergence of microRNAs in Populus. BMC Genomics 8 481
37. GreenwoodMS 1987 Rejuvenation of forest trees. Plant Growth Regul 6 1 12
38. CritchfieldW 1960 Leaf dimorphism in Populus trichocarpa. Am J Bot 47 699 711
39. WangJWSchwabRCzechBMicaEWeigelD 2008 Dual effects of miR156-targeted SPL Genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20 1231 1243
40. AxtellMJBowmanJL 2008 Evolution of plant microRNAs and their targets. Trends Plant Sci 13 343 349
41. YangLConwaySRPoethigRS 2011 Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156. Development 138 245 249
42. DaehlerCCYorkstonMSunWGDudleyN 1999 Genetic variation in morphology and growth characters of Acacia koa in the Hawaiian Islands. Intl J Plant Sci 160 767 773
43. JordanGJPottsBMChalmersPWiltshireRJE 2000 Quantitative genetic evidence that the timing of vegetative phase change in Eucalyptus globulus ssp globulus is an adaptive trait. Aust J Bot 48 561 567
44. JordanGJPottsBMWiltshireRJE 1999 Strong, independent, quantitative genetic control of the timing of vegetative phase change and first flowering in Eucalyptus globulus ssp globulus (Tasmanian Blue Gum). Heredity 83 179 187
45. GreenwoodMS 1995 Juvenility and maturation in conifers - current concepts. Tree Physiol 15 433 438
46. BondBJ 2000 Age-related changes in photosynthesis of woody plants. Trends Plant Sci 5 349 353
47. DayMEGreenwoodMSDiaz-SalaC 2002 Age- and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control. Tree Physiol 22 507 513
48. ChangSPuryearJCairneyJ 1993 A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11 113 116
49. ParkMYWuGGonzalez-SulserAVaucheretHPoethigRS 2005 Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 102 3691 3696
50. TuskanGADiFazioSJanssonSBohlmannJGrigorievI 2006 The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313 1596 1604
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 2
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