Affects Plant Architecture by Regulating Local Auxin Biosynthesis

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Plant architecture is one of the key factors that affect plant survival and productivity. Plant body structure is established through the iterative initiation and outgrowth of lateral organs, which are derived from the shoot apical meristem and root apical meristem, after embryogenesis. Here we report that ADP1, a putative MATE (multidrug and toxic compound extrusion) transporter, plays an essential role in regulating lateral organ outgrowth, and thus in maintaining normal architecture of Arabidopsis. Elevated expression levels of ADP1 resulted in accelerated plant growth rate, and increased the numbers of axillary branches and flowers. Our molecular and genetic evidence demonstrated that the phenotypes of plants over-expressing ADP1 were caused by reduction of local auxin levels in the meristematic regions. We further discovered that this reduction was probably due to decreased levels of auxin biosynthesis in the local meristematic regions based on the measured reduction in IAA levels and the gene expression data. Simultaneous inactivation of ADP1 and its three closest homologs led to growth retardation, relative reduction of lateral organ number and slightly elevated auxin level. Our results indicated that ADP1-mediated regulation of the local auxin level in meristematic regions is an essential determinant for plant architecture maintenance by restraining the outgrowth of lateral organs.

Vyšlo v časopise: Affects Plant Architecture by Regulating Local Auxin Biosynthesis. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1003954
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003954

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Zdroje

1. ReinhardtD, KuhlemeierC (2002) Plant architecture. EMBO Rep 3 : 846–851.

2. WangY, LiJ (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59 : 253–279.

3. PengJ, RichardsDE, HartleyNM, MurphyGP, DevosKM, et al. (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400 : 256–261.

4. LinH, WangR, QianQ, YanM, MengX, et al. (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21 : 1512–1525.

5. JiaoY, WangY, XueD, WangJ, YanM, et al. (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42 : 541–544.

6. WangY, LiJ (2011) Branching in rice. Curr Opin Plant Biol 14 : 94–99.

7. McSteenP, LeyserO (2005) Shoot branching. Annu Rev Plant Biol 56 : 353–374.

8. VannesteS, FrimlJ (2009) Auxin: a trigger for change in plant development. Cell 136 : 1005–1016.

9. NormanlyJ (2010) Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb Perspect Biol 2: a001594.

10. ZhaoY (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61 : 49–64.

11. MashiguchiK, TanakaK, SakaiT, SugawaraS, KawaideH, et al. (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci U S A 108 : 18512–18517.

12. StepanovaAN, AlonsoJM (2011) Bypassing transcription: a shortcut in cytokinin-auxin interactions. Dev Cell 21 : 608–610.

13. ZhaoY (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5 : 334–338.

14. WonC, ShenX, MashiguchiK, ZhengZ, DaiX, et al. (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci U S A 108 : 18518–18523.

15. ZhaoY, ChristensenSK, FankhauserC, CashmanJR, CohenJD, et al. (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291 : 306–309.

16. KimHB, LeeH, OhCJ, LeeNH, AnCS (2007) Expression of EuNOD-ARP1 encoding auxin-repressed protein homolog is upregulated by auxin and localized to the fixation zone in root nodules of Elaeagnus umbellata. Mol Cells 23 : 115–121.

17. ChengY, DaiX, ZhaoY (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20 : 1790–1799.

18. ChengY, QinG, DaiX, ZhaoY (2007) NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis. Proc Natl Acad Sci U S A 104 : 18825–18829.

19. GeislerM, BlakesleeJJ, BouchardR, LeeOR, VincenzettiV, et al. (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44 : 179–194.

20. BlakesleeJJ, BandyopadhyayA, LeeOR, MravecJ, TitapiwatanakunB, et al. (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19 : 131–147.

21. StirnbergP, ChatfieldSP, LeyserHM (1999) AXR1 acts after lateral bud formation to inhibit lateral bud growth in Arabidopsis. Plant Physiol 121 : 839–847.

22. BookerJ, ChatfieldS, LeyserO (2003) Auxin acts in xylem-associated or medullary cells to mediate apical dominance. Plant Cell 15 : 495–507.

23. DharmasiriN, DharmasiriS, WeijersD, LechnerE, YamadaM, et al. (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9 : 109–119.

24. OmoteH, HiasaM, MatsumotoT, OtsukaM, MoriyamaY (2006) The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol Sci 27 : 587–593.

25. SunX, GilroyEM, ChiniA, NurmbergPL, HeinI, et al. (2011) ADS1 encodes a MATE-transporter that negatively regulates plant disease resistance. New Phytol 192 : 471–482.

26. QinG, KangDM, DongYY, ShenYP, ZhangL, et al. (2003) Obtaining and analysis of flanking sequences from T-DNA transformants of Arabidopsis. Plant Sci 165 : 941–949.

27. KurataN, MiyoshiK, NonomuraK, YamazakiY, ItoY (2005) Rice mutants and genes related to organ development, morphogenesis and physiological traits. Plant Cell Physiol 46 : 48–62.

28. GautamPK, RathoreRKS, SutarAR, MangleBB (2011) Characterization of different male sterile lines on morphological characters of India mustard [Brassica juncea (L.) Czern & Coss ] along with their maintainer. Intl Multidiscipl Res J 1 : 4–8.

29. Gomez-RoldanV, FermasS, BrewerPB, Puech-PagesV, DunEA, et al. (2008) Strigolactone inhibition of shoot branching. Nature 455 : 189–194.

30. UmeharaM, HanadaA, YoshidaS, AkiyamaK, AriteT, et al. (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455 : 195–200.

31. YazakiK (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8 : 301–307.

32. HeX, SzewczykP, KaryakinA, EvinM, HongWX, et al. (2010) Structure of a cation-bound multidrug and toxic compound extrusion transporter. Nature 467 : 991–994.

33. VoigtB, TimmersAC, SamajJ, MullerJ, BaluskaF, et al. (2005) GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur J Cell Biol 84 : 595–608.

34. PenalvaMA (2005) Tracing the endocytic pathway of Aspergillus nidulans with FM4-64. Fungal Genet Biol 42 : 963–975.

35. DonaldsonJG, FinazziD, KlausnerRD (1992) Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360 : 350–352.

36. JensenPJ, HangarterRP, EstelleM (1998) Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol 116 : 455–462.

37. UlmasovT, MurfettJ, HagenG, GuilfoyleTJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9 : 1963–1971.

38. LeyserHM, LincolnCA, TimpteC, LammerD, TurnerJ, et al. (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364 : 161–164.

39. AndersenSU, BuechelS, ZhaoZ, LjungK, NovakO, et al. (2008) Requirement of B2-type Cyclin-Dependent Kinases for mersitem integrity in Arabidopsis thaliana. Plant Cell 20 : 88–100.

40. NovakO, HenykovaE, SairanenI, KowalczykM, PospisilT, et al. (2012) Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J 72 : 523–536.

41. OkadaK, UedaJ, KomakiMK, BellCJ, ShimuraY (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3 : 677–684.

42. RomanoCP, RobsonPR, SmithH, EstelleM, KleeH (1995) Transgene-mediated auxin overproduction in Arabidopsis: hypocotyl elongation phenotype and interactions with the hy6-1 hypocotyl elongation and axr1 auxin-resistant mutants. Plant Mol Biol 27 : 1071–1083.

43. KleeHJ, HorschRB, HincheeMA, HeinMB, HoffmannNL (1987) The effects of overproduction of two Agrobacterium tumefaciens T-DNA auxin biosynthetic gene products in transgenic petunia plants. Genes Dev 1 : 86–96.

44. HeislerMG, OhnoC, DasP, SieberP, ReddyGV, et al. (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15 : 1899–1911.

45. KuhlemeierC (2007) Phyllotaxis. Trends Plant Sci 12 : 143–150.

46. BraybrookSA, KuhlemeierC (2010) How a plant builds leaves. Plant Cell 22 : 1006–1018.

47. FrimlJ, YangX, MichniewiczM, WeijersD, QuintA, et al. (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306 : 862–865.

48. PetrasekJ, FrimlJ (2009) Auxin transport routes in plant development. Development 136 : 2675–2688.

49. SauerM, BallaJ, LuschnigC, WisniewskaJ, ReinohlV, et al. (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20 : 2902–2911.

50. BenkovaE, IvanchenkoMG, FrimlJ, ShishkovaS, DubrovskyJG (2009) A morphogenetic trigger: is there an emerging concept in plant developmental biology? Trends Plant Sci 14 : 189–193.

51. BayerEM, SmithRS, MandelT, NakayamaN, SauerM, et al. (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev 23 : 373–384.

52. HeislerMG, HamantO, KrupinskiP, UyttewaalM, OhnoC, et al. (2010) Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol 8: e1000516.

53. MichniewiczM, ZagoMK, AbasL, WeijersD, SchweighoferA, et al. (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130 : 1044–1056.

54. MichniewiczM, BrewerPB, FrimlJI (2007) Polar auxin transport and asymmetric auxin distribution. Arabidopsis Book 5: e0108.

55. GaoX, NagawaS, WangG, YangZ (2008) Cell polarity signaling: focus on polar auxin transport. Mol Plant 1 : 899–909.

56. NohB, MurphyAS, SpaldingEP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13 : 2441–2454.

57. DebeaujonI, PeetersAJ, Leon-KloosterzielKM, KoornneefM (2001) The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 13 : 853–871.

58. DienerAC, GaxiolaRA, FinkGR (2001) Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell 13 : 1625–1638.

59. NawrathC, HeckS, ParinthawongN, MetrauxJP (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14 : 275–286.

60. RogersEE, GuerinotML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14 : 1787–1799.

61. MarinovaK, PourcelL, WederB, SchwarzM, BarronD, et al. (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19 : 2023–2038.

62. MravecJ, SkupaP, BaillyA, HoyerovaK, KreckP, et al. (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459 : 1136–1140.

63. BarbezE, KubesM, RolcikJ, BeziatC, et al. (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485 : 119–122.

64. DingZ, WangB, MorenoI, DuplakovaN, SimonS, et al. (2012) ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat Commun 3 : 941.

65. LiuYG, HangN (1998) Efficient amplification of insert end sequences from bacterial artificial chromosome clones by thermal asymmetric interlaced PCR. Plant Mol Biol Rep 16 : 175–181.

66. QinG, GuH, ZhaoY, MaZ, ShiG, et al. (2005) An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. Plant Cell 17 : 2693–2704.

67. LiuJ, ZhangY, QinG, TsugeT, SakaguchiN, et al. (2008) Targeted degradation of the cyclin-dependent kinase inhibitor ICK4/KRP6 by RING-type E3 ligases is essential for mitotic cell cycle progression during Arabidopsis gametogenesis. Plant Cell 20 : 1538–1554.

68. GuoY, QinG, GuH, QuLJ (2009) Dof5.6/HCA2, a Dof transcription factor gene, regulates interfascicular cambium formation and vascular tissue development in Arabidopsis. Plant Cell 21 : 3518–3534.

69. QinG, MaZ, ZhangL, XingS, HouX, et al. (2007) Arabidopsis AtBECLIN 1/AtAtg6/AtVps30 is essential for pollen germination and plant development. Cell Res 17 : 249–263.

70. ChristieJM, YangH, RichterGL, SullivanS, ThomsonCE, et al. (2011) phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol 9: e1001076.

71. DaiY, WangH, LiB, HuangJ, LiuX, et al. (2006) Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. Plant Cell 18 : 308–320.