A WRKY Transcription Factor Recruits the SYG1-Like Protein SHB1 to Activate Gene Expression and Seed Cavity Enlargement

English version České info

Seed development in Arabidopsis and in many dicots involves an early proliferation of the endosperm to form a large embryo sac or seed cavity close to the size of the mature seed, followed by a second phase during which the embryo grows and replaces the endosperm. SHORT HYPOCOTYL UNDER BLUE1 (SHB1) is a member of the SYG1 protein family in fungi, Caenorhabditis elegans, flies, and mammals. SHB1 gain-of-function enhances endosperm proliferation, increases seed size, and up-regulates the expression of the WRKY transcription factor gene MINISEED3 (MINI3) and the LRR receptor kinase gene HAIKU2 (IKU2). Mutations in either IKU2 or MINI3 retard endosperm proliferation and reduce seed size. However, the molecular mechanisms underlying the establishment of the seed cavity and hence the seed size remain largely unknown. Here, we show that the expression of MINI3 and IKU2 is repressed before fertilization and after 4 days after pollination (DAP), but is activated by SHB1 from 2 to 4 DAP prior to the formation of the seed cavity. SHB1 associates with their promoters but without a recognizable DNA binding motif, and this association is abolished in mini3 mutant. MINI3 binds to W-boxes in, and recruits SHB1 to, its own and IKU2 promoters. Interestingly, SHB1, but not MINI3, activates transcription of pMINI3::GUS or pIKU2::GUS. We reveal a critical developmental switch through the activation of MINI3 expression by SHB1. The recruitment of SHB1 by MINI3 to its own and IKU2 promoters represents a novel two-step amplification to counter the low expression level of IKU2, which is a trigger for endosperm proliferation and seed cavity enlargement.

Vyšlo v časopise: A WRKY Transcription Factor Recruits the SYG1-Like Protein SHB1 to Activate Gene Expression and Seed Cavity Enlargement. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003347
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003347

Souhrn

Zdroje

1. SundaresanV (2005) Control of seed size in plants. Proc Natl Acad Sci USA 102 : 17887–17888.

2. SunX, ShantharajD, KangX, NiM (2010) Transcriptional and hormonal signaling control of Arabidopsis seed development. Curr Opin Plant Biol 13 : 611–620.

3. Boisnard-LorigC, Colon-CarmonaA, BauchM, HodgeS, DoernerP, et al. (2001) YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell 13 : 495–509.

4. OlsenOA (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Phys Plant Mol Biol 52 : 233–267.

5. BergerF (2003) Endosperm, the crossroad of seed development. Curr Opin Plant Biol 6 : 42–50.

6. GarciaD, SaingeryV, ChambrierP, MayerU, JurgensG, et al. (2003) Arabidopsis haiku mutants reveal new controls of seed size by endosperm. Plant Physiol 131 : 1661–1670.

7. ScottRJ, SpielmanM, BaileyJ, DickinsonHG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125 : 3329–3341.

8. GarciaD, Fitz GeraldJN, BergerF (2005) Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell 17 : 52–60.

9. XiaoW, BrownRC, LemmonBE, HaradaJJ, GoldbergRB, et al. (2006) Regulation of seed size by hypomethylation of maternal and paternal genomes. Plant Physiol 142 : 1160–1168.

10. JofukuKD, OmidyarPK, GeeZ, OkamuroJK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc. Natl. Acd. Sci. USA 102 : 3117–3122.

11. OhtoM, FischerRL, GoldbergRB, NakamuraK, HaradaJJ (2005) Control of seed mass by APETALA2. Proc. Natl. Acd. Sci. USA 102 : 3123–3128.

12. LuoM, ElizabethS, DennisES, BergerF, PeacockWJ, et al. (2005) MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc Natl Acd Sci USA 102 : 17531–17536.

13. FitzGeraldJ, LuoM, ChaudhuryA, BergerF (2008) DNA methylation causes predominant maternal controls of plant embryo growth. PLoS ONE 3: e2298 doi:10.1371/journal.pone.0002298.

14. SchruffMC, SpielmanM, TiwariS, AdamsS, FenbyN, et al. (2005) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133 : 251–261.

15. ZhouY, ZhangX, KangX, ZhaoX, ZhangX, et al. (2009) SHORT HYPOCOTYL UNDER BLUE1 associates with MINISEED3 and HAIKU2 promoters in vivo to control Arabidopsis seed development. Plant Cell 21 : 106–117.

16. WangA, GarciaD, ZhangH, FengK, ChaudhuryA, et al. (2010) The VQ motif protein IKU1 regulates endosperm growth and seed size in Arabidopsis. Plant J 63 : 670–679.

17. KangX, NiM (2006) Arabidopsis SHORT HYPOCOTYL UNDER BLUE 1 contains SPX and EXS domains and acts in cryptochrome signaling. Plant Cell 18 : 921–934.

18. KangIH, SteffenJG, PortereikoMF, LloydA, DrewsGN (2008) The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20 : 635–647.

19. SpainBH, KooD, RamakrishnanM, DzudzorB, ColicelliJ (1995) Truncated forms of a novel yeast protein suppress the lethality of a G protein α subunit deficiency by interacting with the β subunit. J Biol Chem 270 : 25435–25444.

20. CiolkowskiI, WankeD, BirkenbihlRP, SomssichIE (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 68 : 81–92.

21. TailorCS, NouriA, LeeCG, KozakC, KabatD (1999) Cloning and characterization of a cell surface receptor for xenotropic and polytropic murine leukemia viruses. Proc Natl Acad Sci USA 96 : 927–932.

22. YangYL, GuoL, XuS, HollandCA, KitamuraT, et al. (1999) Receptors for polytropic and xenotropic mouse leukemia viruses encoded by a single gene at Rmc1. Nat Genet 21 : 216–219.

23. EulgemT, RushtonPJ, RobatzekS, SomssichIE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5 : 199–206.

24. HellensRP, AllanAC, FrielEN, BolithoK, GraftonK, et al. (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1 : 13 doi:10.1186/1746-4811-1-13.

25. RiechmannJL, MeyerowitzEM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379 : 633–646.

26. OhtoMA, FloydSK, FischerRL, GoldbergRB, HaradaJJ (2009) Effects of APETALA2 on embryo, endosperm, and seed coat development determine seed size in Arabidopsis. Sex Plant Reprod 22 : 277–289.

27. PortereikoMF, LloydA, SteffenJG, PunwaniJA, OtsugaD, et al. (2006) AGL80 is required for central cell and endosperm development in Arabidopsis. Plant Cell 18 : 1862–1872.

28. SteffenJG, KangIH, PortereikoMF, LloydA, DrewsGN (2008) AGL61 interacts with AGL80 and is required for central cell development in Arabidopsis. Plant Physiol 148 : 259–268.

29. de FolterS, ImminkRG, KiefferM, ParenicováL, HenzSR, et al. (2005) Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17 : 1424–1433.

30. HennigL, DerkachevaM (2009) Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25 : 414–423.

31. LuoM, BilodeauP, DennisES, PeacockWJ, ChaudhuryA (2000) Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci USA 97 : 10637–10642.

32. XiaoW, GehringM, ChoiY, MargossianL, PuH, et al. (2003) Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell 5 : 891–901.

33. CurtisMD, GrossniklausU (2003) A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta. Plant Physiol 133 : 462–469.

34. BentA, KunkelB, DahlbeckD, BrownK, SchmidtR, et al. (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265 : 1856–1860.

35. BowlerC, BenvenutoG, LaflammeP, MolinoD, ProbstAV, et al. (2004) Chromatin techniques for plant cells. Plant J 39 : 776–789.

36. SunX, NiM (2011) HYPOSENSITIVE TO LIGHT, an Alpha/Beta Fold Protein, Acts Downstream of ELONGATED HYPOCOTYL 5 to Regulate Seedling De-Etiolation. Mol Plant 4 : 116–126.

37. EarleyKW, HaagJR, PontesO, OpperK, JuehneT, et al. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45 : 616–629.

38. TangW, YuanM, WangR, YangY, WangC, et al. (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13 : 124–131.

39. SunX, KangX, NiM (2012) Hypersensitive to Red and Blue 1 and its modification by Protein Phosphatase 7 are implicated in the control of Arabidopsis stomatal aperture. PLoS Genet 8: e1002674 doi:10.1371/journal.pgen.1002674.

40. ZhouY, NiM (2010) SHB1 truncations and mutations alter its association with a signaling protein complex. Plant Cell 22 : 703–715.

41. WydroM, KozubekE, LehmannP (2006) Optimization of transient Agrobacterium-mediated gene expression system in leaves of Nicotiana benthamiana. Acta Biochim Pol 53 : 289–298.

42. SessaG, BorelloU, MorelliG, RubertiI (1998) A Transient Assay for Rapid Functional Analysis of Transcription Factors in Arabidopsis. Plant Mol Biol Rep 16 : 191–197.