#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Atkinesin-13A Modulates Cell-Wall Synthesis and Cell Expansion in via the THESEUS1 Pathway


Most of the visible growth of plant organs is driven by cell expansion without associated cell division. As plant cells are encased in cell walls, expansion requires the controlled loosening of the existing cell wall and synthesis of additional wall material. While a number of factors and plant hormones are known that promote cell expansion, what limits this process and thus restricts final cell and organ size is less well understood. Here, we identify a mutant that forms larger flowers because of increased cell expansion. The affected gene encodes a motor protein associated with the microtubule cytoskeleton that causes microtubule break-down and is required for ensuring an even distribution of secretory organelles within cells. Reduced activity of this motor protein triggers the activation of a pathway that detects defects in cell-wall integrity, which in turn leads to the observed increase in cell-wall synthesis and expansion. The Arabidopsis genome encodes another highly similar motor protein, and the combined loss of their activities causes severe defects, including reduced cell expansion. Thus, the two proteins fulfill an essential function in plant cell growth, and their full activity appears to be required to ensure normal cell-wall synthesis and a timely cessation of cell expansion.


Vyšlo v časopise: Atkinesin-13A Modulates Cell-Wall Synthesis and Cell Expansion in via the THESEUS1 Pathway. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004627
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004627

Souhrn

Most of the visible growth of plant organs is driven by cell expansion without associated cell division. As plant cells are encased in cell walls, expansion requires the controlled loosening of the existing cell wall and synthesis of additional wall material. While a number of factors and plant hormones are known that promote cell expansion, what limits this process and thus restricts final cell and organ size is less well understood. Here, we identify a mutant that forms larger flowers because of increased cell expansion. The affected gene encodes a motor protein associated with the microtubule cytoskeleton that causes microtubule break-down and is required for ensuring an even distribution of secretory organelles within cells. Reduced activity of this motor protein triggers the activation of a pathway that detects defects in cell-wall integrity, which in turn leads to the observed increase in cell-wall synthesis and expansion. The Arabidopsis genome encodes another highly similar motor protein, and the combined loss of their activities causes severe defects, including reduced cell expansion. Thus, the two proteins fulfill an essential function in plant cell growth, and their full activity appears to be required to ensure normal cell-wall synthesis and a timely cessation of cell expansion.


Zdroje

1. PowellAE, LenhardM (2012) Control of organ size in plants. Curr Biol 22: R360–367.

2. Sugimoto-ShirasuK, RobertsK (2003) “Big it up”: Endoreduplication and cell-size control in plants. Curr Opin Plant Biol 6: 544–553.

3. MelaragnoJE, MehrotraB, ColemanAW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5: 1661–1668.

4. Taiz L, Zeiger E (2010) Plant physiology. Sunderland, MA: Sinauer Associates.

5. WoltersH, JurgensG (2009) Survival of the flexible: Hormonal growth control and adaptation in plant development. Nat Rev Genet 10: 305–317.

6. BaiMY, FanM, OhE, WangZY (2012) A triple helix-loop-helix/basic helix-loop-helix cascade controls cell elongation downstream of multiple hormonal and environmental signaling pathways in Arabidopsis. Plant Cell 24: 4917–4929.

7. IkedaM, FujiwaraS, MitsudaN, Ohme-TakagiM (2012) A triantagonistic basic helix-loop-helix system regulates cell elongation in Arabidopsis. Plant Cell 24: 4483–4497.

8. HuY, PohHM, ChuaNH (2006) The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth. Plant J 47: 1–9.

9. DeprostD, YaoL, SormaniR, MoreauM, LeterreuxG, et al. (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mrna translation. EMBO Rep 8: 864–870.

10. MenandB, DesnosT, NussaumeL, BergerF, BouchezD, et al. (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci U S A 99: 6422–6427.

11. Menand B, Robaglia C (2004) Plant cell growth. In: Hall MN, editor. Cell growth: Control of cell size. 01 ed. New York: Cold Spring Harbor Laboratory Press. pp. 625–637.

12. BrioudesF, JolyC, SzecsiJ, VaraudE, LerouxJ, et al. (2009) Jasmonate controls late development stages of petal growth in Arabidopsis thaliana. Plant J 60: 1070–1080.

13. SzecsiJ, JolyC, BordjiK, VaraudE, CockJM, et al. (2006) BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size. Embo J 25: 3912–3920.

14. VaraudE, BrioudesF, SzecsiJ, LerouxJ, BrownS, et al. (2011) AUXIN RESPONSE FACTOR8 regulates Arabidopsis petal growth by interacting with the bHLH transcription factor BIGPETALp. Plant Cell 23: 973–983.

15. CosgroveDJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6: 850–861.

16. ChoHT, CosgroveDJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci U S A 97: 9783–9788.

17. ChoiD, LeeY, ChoHT, KendeH (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15: 1386–1398.

18. ZenoniS, RealeL, TornielliGB, LanfaloniL, PorcedduA, et al. (2004) Downregulation of the Petunia hybrida alpha-expansin gene PhEXP1 reduces the amount of crystalline cellulose in cell walls and leads to phenotypic changes in petal limbs. Plant Cell 16: 295–308.

19. SomervilleC (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22: 53–78.

20. PerssonS, ParedezA, CarrollA, PalsdottirH, DoblinM, et al. (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci U S A 104: 15566–15571.

21. CrowellEF, BischoffV, DesprezT, RollandA, StierhofYD, et al. (2009) Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21: 1141–1154.

22. GutierrezR, LindeboomJJ, ParedezAR, EmonsAM, EhrhardtDW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11: 797–806.

23. ParedezAR, SomervilleCR, EhrhardtDW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312: 1491–1495.

24. WightmanR, TurnerS (2010) Trafficking of the plant cellulose synthase complex. Plant Physiol 153: 427–432.

25. SampathkumarA, GutierrezR, McFarlaneHE, BringmannM, LindeboomJ, et al. (2013) Patterning and lifetime of plasma membrane-localized cellulose synthase is dependent on actin organization in Arabidopsis interphase cells. Plant Physiol 162: 675–688.

26. BringmannM, LiE, SampathkumarA, KocabekT, HauserMT, et al. (2012) POM-POM2/cellulose synthase interacting1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24: 163–177.

27. LuL, LeeYR, PanR, MaloofJN, LiuB (2005) An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol Biol Cell 16: 811–823.

28. ZhongR, BurkDH, MorrisonWH3rd, YeZH (2002) A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14: 3101–3117.

29. WeiL, ZhangW, LiuZ, LiY (2009) AtKinesin-13a is located on Golgi-associated vesicle and involved in vesicle formation/budding in Arabidopsis root-cap peripheral cells. BMC Plant Biol 9: 138.

30. SmithLG, OppenheimerDG (2005) Spatial control of cell expansion by the plant cytoskeleton. Annu Rev Cell Dev Biol 21: 271–295.

31. OdaY, FukudaH (2013) Rho of plant GTPase signaling regulates the behavior of Arabidopsis kinesin-13a to establish secondary cell wall patterns. Plant Cell 25: 4439–4450.

32. OdaY, FukudaH (2013) The dynamic interplay of plasma membrane domains and cortical microtubules in secondary cell wall patterning. Front Plant Sci 4: 511.

33. FolkersU, KirikV, SchobingerU, FalkS, KrishnakumarS, et al. (2002) The cell morphogenesis gene ANGUSTIFOLIA encodes a CtBP/BARS-like protein and is involved in the control of the microtubule cytoskeleton. Embo J 21: 1280–1288.

34. KimGT, ShodaK, TsugeT, ChoKH, UchimiyaH, et al. (2002) The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. Embo J 21: 1267–1279.

35. MinamisawaN, SatoM, ChoKH, UenoH, TakechiK, et al. (2011) ANGUSTIFOLIA, a plant homolog of CtBP/BARS, functions outside the nucleus. Plant J 68: 788–799.

36. HamannT, DennessL (2011) Cell wall integrity maintenance in plants: Lessons to be learned from yeast? Plant Signal Behav 6: 1706–1709.

37. KohornBD, JohansenS, ShishidoA, TodorovaT, MartinezR, et al. (2009) Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J 60: 974–982.

38. KohornBD, KobayashiM, JohansenS, RieseJ, HuangLF, et al. (2006) An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. Plant J 46: 307–316.

39. WagnerTA, KohornBD (2001) Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13: 303–318.

40. Boisson-DernierA, KesslerSA, GrossniklausU (2011) The walls have ears: The role of plant CrRLK1Ls in sensing and transducing extracellular signals. J Exp Bot 62: 1581–1591.

41. HematyK, SadoPE, Van TuinenA, RochangeS, DesnosT, et al. (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17: 922–931.

42. GuoH, LiL, YeH, YuX, AlgreenA, et al. (2009) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci U S A 106: 7648–7653.

43. AlonsoJM, StepanovaAN, LeisseTJ, KimCJ, ChenH, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657.

44. HoriguchiG, FujikuraU, FerjaniA, IshikawaN, TsukayaH (2006) Large-scale histological analysis of leaf mutants using two simple leaf observation methods: Identification of novel genetic pathways governing the size and shape of leaves. Plant J 48: 638–644.

45. RobbinsCT, MoenAN (1975) Composition and digestibility of several deciduous browses in the northeast. The Journal of Wildlife Management 39: 337–341.

46. GendreauE, TraasJ, DesnosT, GrandjeanO, CabocheM, et al. (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114: 295–305.

47. ClouseSD, LangfordM, McMorrisTC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111: 671–678.

48. GuzmanP, EckerJR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513–523.

49. TsugeT, TsukayaH, UchimiyaH (1996) Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (l.) heynh. Development 122: 1589–1600.

50. KimGT, FujiokaS, KozukaT, TaxFE, TakatsutoS, et al. (2005) CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J 41: 710–721.

51. AndersonCT, CarrollA, AkhmetovaL, SomervilleC (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152: 787–796.

52. LandreinB, LatheR, BringmannM, VouillotC, IvakovA, et al. (2013) Impaired cellulose synthase guidance leads to stem torsion and twists phyllotactic patterns in Arabidopsis. Curr Biol 23: 895–900.

53. WinterD, VinegarB, NahalH, AmmarR, WilsonGV, et al. (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2: e718.

54. SchwabR, OssowskiS, WarthmannN, WeigelD (2010) Directed gene silencing with artificial microRNAs. Methods Mol Biol 592: 71–88.

55. RoslanHA, SalterMG, WoodCD, WhiteMR, CroftKP, et al. (2001) Characterization of the ethanol-inducible alc gene-expression system in Arabidopsis thaliana. Plant J 28: 225–235.

56. MuchaE, HoefleC, HuckelhovenR, BerkenA (2010) RIP3 and AtKinesin-13A - a novel interaction linking rho proteins of plants to microtubules. Eur J Cell Biol 89: 906–916.

57. ManeyT, WagenbachM, WordemanL (2001) Molecular dissection of the microtubule depolymerizing activity of mitotic centromere-associated kinesin. The Journal of biological chemistry 276: 34753–34758.

58. MooresCA, MilliganRA (2006) Lucky 13 - microtubule depolymerisation by kinesin-13 motors. J Cell Sci 119: 3905–3913.

59. JanderG, NorrisSR, RounsleySD, BushDF, LevinIM, et al. (2002) Arabidopsis map-based cloning in the post-genome era. Plant Physiol 129: 440–450.

60. DischS, AnastasiouE, SharmaVK, LauxT, FletcherJC, et al. (2006) The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr Biol 16: 272–279.

61. CloughSJ, BentAF (1998) Floral dip: A simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743.

62. BeckerD, KemperE, SchellJ, MastersonR (1992) New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol Biol 20: 1195–1197.

63. LodwigEM, LeonardM, MarroquiS, WheelerTR, FindlayK, et al. (2005) Role of polyhydroxybutyrate and glycogen as carbon storage compounds in pea and bean bacteroids. Mol Plant Microbe Interact 18: 67–74.

64. DerbyshireP, FindlayK, McCannMC, RobertsK (2007) Cell elongation in Arabidopsis hypocotyls involves dynamic changes in cell wall thickness. J Exp Bot 58: 2079–2089.

65. HinchaDK, ZutherE, HellwegeEM, HeyerAG (2002) Specific effects of fructo- and gluco-oligosaccharides in the preservation of liposomes during drying. Glycobiology 12: 103–110.

66. KemsleyEK (1996) Discriminant analysis of high-dimensional data: A comparison of principal components analysis and partial least squares data reduction methods. Chemometrics and Intelligent Laboratory Systems 33: 47–61.

67. McCannMC, DefernezM, UrbanowiczBR, TewariJC, LangewischT, et al. (2007) Neural network analyses of infrared spectra for classifying cell wall architectures. Plant Physiol 143: 1314–1326.

68. Sanchez-RodriguezC, BauerS, HematyK, SaxeF, IbanezAB, et al. (2012) Chitinase-like1/pom-pom1 and its homolog CTL2 are glucan-interacting proteins important for cellulose biosynthesis in Arabidopsis. Plant Cell 24: 589–607.

69. Dische Z (1962) General color reactions. RL Whistler and ML Wolfrom, Editors, Methods in Carbohydrate Chemistry, Academic Press, New York: 478–481.

70. FilisetticozziTMCC, CarpitaNC (1991) Measurement of uronic-acids without interference from neutral sugars. Analytical Biochemistry 197: 157–162.

71. SmythDR, BowmanJL, MeyerowitzEM (1990) Early flower development in Arabidopsis. Plant Cell 2: 755–767.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#