SHINE Transcription Factors Act Redundantly to Pattern the Archetypal Surface of Arabidopsis Flower Organs

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Floral organs display tremendous variation in their exterior that is essential for organogenesis and the interaction with the environment. This diversity in surface characteristics is largely dependent on the composition and structure of their coating cuticular layer. To date, mechanisms of flower organ initiation and identity have been studied extensively, while little is known regarding the regulation of flower organs surface formation, cuticle composition, and its developmental significance. Using a synthetic microRNA approach to simultaneously silence the three SHINE (SHN) clade members, we revealed that these transcription factors act redundantly to shape the surface and morphology of Arabidopsis flowers. It appears that SHNs regulate floral organs' epidermal cell elongation and decoration with nanoridges, particularly in petals. Reduced activity of SHN transcription factors results in floral organs' fusion and earlier abscission that is accompanied by a decrease in cutin load and modified cell wall properties. SHN transcription factors possess target genes within four cutin- and suberin-associated protein families including, CYP86A cytochrome P450s, fatty acyl-CoA reductases, GSDL-motif lipases, and BODYGUARD1-like proteins. The results suggest that alongside controlling cuticular lipids metabolism, SHNs act to modify the epidermis cell wall through altering pectin metabolism and structural proteins. We also provide evidence that surface formation in petals and other floral organs during their growth and elongation or in abscission and dehiscence through SHNs is partially mediated by gibberellin and the DELLA signaling cascade. This study therefore demonstrates the need for a defined composition and structure of the cuticle and cell wall in order to form the archetypal features of floral organs surfaces and control their cell-to-cell separation processes. Furthermore, it will promote future investigation into the relation between the regulation of organ surface patterning and the broader control of flower development and biological functions.

Vyšlo v časopise: SHINE Transcription Factors Act Redundantly to Pattern the Archetypal Surface of Arabidopsis Flower Organs. PLoS Genet 7(5): e32767. doi:10.1371/journal.pgen.1001388
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001388

Souhrn

Zdroje

1. TaizL

ZeigerE

2002 Plant Physiology Sunderland, MA Sinauer Associates, Inc 672

2. KolattukudyPE

2001 Polyesters in higher plants. Adv Biochem Eng Biotechnol 71 1 49

3. JeffreeCE

1996 Structure and ontogeny of plant cuticle Oxford BIOS Scientific Publishers 33 83

4. KutscheraU

NiklasKJ

2007 The epidermal-growth-control theory of stem elongation: An old and a new perspective. J Plant Physiol 164 1395 1409

5. Savaldi-GoldsteinS

PetoC

ChoryJ

2007 The epidermis both drives and restricts plant shoot growth. Nature 446 199 202

6. BachL

FaureJD

2010 Role of very-long-chain fatty acids in plant development, when chain length does matter. Comptes Rendus Biologies 333 361 370

7. Reina-PintoJJ

YephremovA

2009 Surface lipids and plant defenses. Plant Physiol Biochem 47 540 549

8. NawrathC

2002 The biopolymer cutin and suberin.

SomervilleCR

MyerowitzEM

The Arabidopsis Book Rockville American Society of Plant Biologists

9. SuhMC

SamuelsAL

JetterR

KunstL

PollardM

2005 Cuticular lipid composition, surface structure, and gene expression in Arabidopsis stem epidermis. Plant Physiol 139 1649 1665

10. PollardM

BeissonF

LiYH

OhlroggeJB

2008 Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13 236 246

11. SamuelsL

KunstL

JetterR

2008 Sealing plant surfaces: Cuticular wax formation by epidermal cells. Ann Rev Plant Biol 59 683 707

12. SandhuAP

RandhawaGS

DhuggaKS

2009 Plant cell wall matrix polysaccharide biosynthesis. Mol Plant 2 840 850

13. AndersonCM

WagnerTA

PerretM

HeZH

HeDZ

2001 WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol Biol 47 197 206

14. CaffallKH

MohnenD

2009 The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohyd Res 344 1879 1900

15. BrounP

2004 Transcription factors as tools for metabolic engineering in plants. Curr Opin Plant Biol 7 202 209

16. AharoniA

DixitS

JetterR

ThoenesE

van ArkelG

2004 The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16 2463 2480

17. BrounP

PoindexterP

OsborneE

JiangCZ

RiechmannJL

2004 WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA 101 4706 4711

18. KannangaraR

BraniganC

LiuY

PenfieldT

RaoV

2007 The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19 1278 1294

19. TaketaS

AmanoS

TsujinoY

SatoT

SaishoD

2008 Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway. Proc Natl Acad Sci USA 105 4062 4067

20. LolleSJ

HsuW

PruittRE

1998 Genetic analysis of organ fusion in Arabidopsis thaliana. Genetics 149 607 619

21. PanikashviliD

ShiJX

BocobzaS

FrankeRB

SchreiberL

2010 The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Mol Plant 3 563 575

22. PanikashviliD

ShiJX

SchreiberL

AharoniA

2009 The Arabidopsis DCR encoding a soluble BAHD acyltransferase is required for cutin polyester formation and seed hydration properties. Plant Physiol 151 1773 1789

23. Li-BeissonY

PollardM

SauveplaneV

PinotF

OhlroggeJ

2009 Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester. Proc Natl Acad Sci USA

24. KurdyukovS

FaustA

NawrathC

BarS

VoisinD

2006 The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 18 321 339

25. DomergueF

VishwanathSJ

JoubesJ

OnoJ

LeeJA

Three Arabidopsis fatty acyl-CoA reductases, FAR1, FAR4, and FAR5, generate primary fatty alcohols associated with suberin deposition. Plant Physiol 153 1539 1554

26. AhnSJ

ShinR

SchachtmanDP

2004 Expression of KT/KUP genes in arabidopsis and the role of root hairs in K+ uptake. Plant Physiol 134 1135 1145

27. RuanYL

LlewellynDJ

FurbankRT

2001 The control of single-celled cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13 47 60

28. GeislerM

MurphyAS

2006 The ABC of auxin transport: The role of p-glycoproteins in plant development. FEBS Lett 580 1094 1102

29. SeifertGJ

BlaukopfC

2010 Irritable walls: The plant extracellular matrix and signaling. Plant Physiol 153 467 478

30. GouJY

ParkS

YuXH

MillerLM

LiuCJ

2008 Compositional characterization and imaging of “wall-bound” acylesters of Populus trichocarpa reveal differential accumulation of acyl molecules in normal and reactive woods. Planta 229 15 24

31. FellahA

AnjukandiP

WaterlandMR

WilliamsMAK

2009 Determining the degree of methylesterification of pectin by ATR/FT-IR: Methodology optimisation and comparison with theoretical calculations. Carbohyd Polym 78 847 853

32. SeneC

McCannMC

WilsonRH

GrinterR

1994 Fourier-transform raman and fourier-transform infrared spectroscopy (an investigation of five higher plant cell walls and their components). Plant Physiol 106 1623 1631

33. YuP

2005 Molecular chemistry imaging to reveal structural features of various plant feed tissues. J Struct Biol 150 81 89

34. VerhertbruggenY

MarcusSE

HaegerA

Ordaz-OrtizJJ

KnoxJP

2009 An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohyd Res 344 1858 1862

35. ZimmermannP

Hirsch-HoffmannM

HennigL

GruissemW

2004 GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136 2621 2632

36. WagstaffC

YangTJW

SteadAD

Buchanan-WollastonV

RobertsJA

2009 A molecular and structural characterization of senescing Arabidopsis siliques and comparison of transcriptional profiles with senescing petals and leaves. Plant J 57 690 705

37. CaiSQ

LashbrookCC

2008 Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: Enhanced retention of floral organs in Transgenic plants overexpressing Arabidopsis ZINC FINGER PROTEIN2. Plant Physiology 146 1305 1321

38. KramBW

XuWW

CarterCJ

2009 Uncovering the Arabidopsis thaliana nectary transcriptome: investigation of differential gene expression in floral nectariferous tissues. BMC Plant Biol 9 92

39. NaranjoMA

FormentJ

RoldanM

SerranoR

VicenteO

2006 Overexpression of Arabidopsis thaliana LTL1, a salt-induced gene encoding a GDSL-motif lipase, increases salt tolerance in yeast and transgenic plants. Plant Cell Environ 29 1890 1900

40. HellensRP

AllanAC

FrielEN

BolithoK

GraftonK

2005 Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1 13

41. YuH

ItoT

ZhaoYX

PengJR

KumarPP

2004 Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci USA 101 7827 7832

42. CaoDN

ChengH

WuW

SooHM

PengJR

2006 Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol 142 509 525

43. WilsonRN

HeckmanJW

SCR

1992 Gibberelellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100 403 408

44. MartinC

GloverBJ

2007 Functional aspects of cell patterning in aerial epidermis. Curr Opin Plant Biol 10 70 82

45. WhitneyHM

ChittkaL

BruceTJ

GloverBJ

2009 Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Curr Biol 19 948 953

46. IrishVF

2010 The flowering of Arabidopsis flower development. Plant J 61 1014 1028

47. SaladieM

MatasAJ

IsaacsonT

JenksMA

GoodwinSM

2007 A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiol 144 1012 1028

48. WolfS

MouilleG

PellouxJ

2009 Homogalacturonan methyl-esterification and plant development. Mole Plant 2 851 860

49. FarrokhiN

BurtonRA

BrownfieldL

HrmovaM

WilsonSM

2006 Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol J 4 145 167

50. OgawaM

KayP

WilsonS

SwainSM

2009 ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are Polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21 216 233

51. DobritsaAA

ShresthaJ

MorantM

PinotF

MatsunoM

2009 CYP704B1 is a long-chain fatty acid omega-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151 574 589

52. LiH

PinotF

SauveplaneV

Werck-ReichhartbD

DiehlP

2010 Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22 173 190

53. PinotF

BeissonF

2011 Cytochrome P450 metabolizing fatty acids in plants: characterization and physiological roles. FEBS J 278 195 205

54. FrankeR

BriesenI

WojciechowskiT

FaustA

YephremovA

2005 Apoplastic polyesters in Arabidopsis surface tissues–a typical suberin and a particular cutin. Phytochemistry 66 2643 2658

55. FrankeR

HoferR

BriesenI

EmsermannM

EfremovaN

2009 The DAISY gene from Arabidopsis encodes a fatty acid elongase condensing enzyme involved in the biosynthesis of aliphatic suberin in roots and the chalaza-micropyle region of seeds. Plant J 57 80 95

56. BaxterI

HosmaniPS

RusA

LahnerB

BorevitzJO

2009 Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet 5 e1000492 doi:10.1371/journal.pgen.1000492

57. HoeferR

BriesenI

BeckM

PinotF

SchreiberL

2008 The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid omega-hydroxylase involved in suberin monomer biosynthesis. J Exp Bot 59 2347 2360

58. LeeEJ

MatsumuraY

SogaK

HosonT

KoizumiN

2007 Glycosyl hydrolases of cell wall are induced by sugar starvation in Arabidopsis. Plant Cell Physiol 48 405 413

59. HovavR

UdallJA

HovavE

RappR

FlagelL

2008 A majority of cotton genes are expressed in single-celled fiber. Planta 227 319 329

60. ChaudharyB

HovavR

FlagelL

MittlerR

WendelJF

2009 Parallel expression evolution of oxidative stress-related genes in fiber from wild and domesticated diploid and polyploid cotton (Gossypium). BMC Genomics 10 378

61. LeeJJ

WoodwardAW

ChenZJ

2007 Gene expression changes and early events in cotton fibre development. Ann Bot 100 1391 1401

62. ChengH

QinLJ

LeeSC

FuXD

RichardsDE

2004 Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131 1055 1064

63. Mutasa-GottgensE

HeddenP

2009 Gibberellin as a factor in floral regulatory networks. J Exp Bot 60 1979 1989

64. HoffmannbenningS

KendeH

1994 Cuticle Biosynthesis in rapidly growing internodes of deep-water rice. Plant Physiol 104 719 723

65. BowenDJ

WaltonTJ

1988 Cutin Composition and Biosynthesis during Gibberellic Acid-Induced Stem Extension of Pisum-Sativum Var Meteor. Plant Sci 55 115 127

66. KnocheM

BeyerM

PeschelS

OparlakovB

BukovacMJ

2004 Changes in strain and deposition of cuticle in developing sweet cherry fruit. Physiol Plantarum 120 667 677

67. HisamatsuT

KingRW

2008 The nature of floral signals in Arabidopsis. II. Roles for FLOWERING LOCUS T (FT) and gibberellin. Journal of Experimental Botany 59 3821 3829

68. CloughSJ

BentAF

1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J16 735 743

69. TanakaT

TanakaH

MachidaC

WatanabeM

MachidaY

2004 A new method for rapid visualization of defects in leaf cuticle reveals five intrinsic patterns of surface defects in Arabidopsis. Plant J 37 139 146

70. McCartneyL

Steele-KingCG

JordanE

KnoxJP

2003 Cell wall pectic (1–4)-beta-D-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J 33 447 454

71. WeigelD

GlazebrookJ

2002 Arabidopsis: A Laboratory Manual: Cold Spring Harbor Laboratory Press

72. ChuartzmanSG

NevoR

ShimoniE

CharuviD

KissV

2008 Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20 1029 1039

73. IrizarryRA

HobbsB

CollinF

Beazer-BarclayYD

AntonellisKJ

2003 Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 249 264

74. VogelJP

RaabTK

SchiffC

SomervilleSC

2002 PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14 2095 2106

75. WillatsWGT

GilmartinPM

MikkelsenJD

KnoxJP

1999 Cell wall antibodies without immunization: generation and use of de-esterified homogalacturonan block-specific antibodies from a naive phage display library. Plant J 18 57 65

76. VoinnetO

RivasS

MestreP

BaulcombeD

2003 An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33 949 956