Spatiotemporal cytoskeleton organizations determine morphogenesis of multicellular trichomes in tomato

Autoři: Jiang Chang aff001;  Zhijing Xu aff001;  Meng Li aff001;  Meina Yang aff001;  Haiyang Qin aff001;  Jie Yang aff001;  Shuang Wu aff001
Působiště autorů: College of Horticulture, FAFU-UCR Joint Center and Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, China aff001
Vyšlo v časopise: Spatiotemporal cytoskeleton organizations determine morphogenesis of multicellular trichomes in tomato. PLoS Genet 15(10): e1008438. doi:10.1371/journal.pgen.1008438
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008438


Plant trichomes originate from epidermal cell, forming protective structure from abiotic and biotic stresses. Different from the unicellular trichome in Arabidopsis, tomato trichomes are multicellular structure and can be classified into seven different types based on cell number, shape and the presence of glandular cells. Despite the importance of tomato trichomes in insect resistance, our understanding of the tomato trichome morphogenesis remains elusive. In this study, we quantitatively analyzed morphological traits of trichomes in tomato and further performed live imaging of cytoskeletons in stably transformed lines with actin and microtubule markers. At different developmental stages, two types of cytoskeletons exhibited distinct patterns in different trichome cells, ranging from transverse, spiral to longitudinal. This gradual transition of actin filament angle from basal to top cells could correlate with the spatial expansion mode in different cells. Further genetic screen for aberrant trichome morphology led to the discovery of a number of independent mutations in SCAR/WAVE and ARP2/3 complex, which resulted in actin bundling and distorted trichomes. Disruption of microtubules caused isotropic expansion while abolished actin filaments entirely inhibited axial extension of trichomes, indicating that microtubules and actin filaments may control distinct aspects of trichome cell expansion. Our results shed light on the roles of cytoskeletons in the formation of multicellular structure of tomato trichomes.

Klíčová slova:

Actins – Anisotropy – Microtubules – Tomatoes – Trichomes – Actin filaments – Cytoskeleton – Basal cells


1. Powell AE, Lenhard M. Control of organ size in plants. Curr Biol, 2012, 22: R360–R367. doi: 10.1016/j.cub.2012.02.010 22575478

2. Tsukaya M. Mechanism of leaf-shape determination. Annu Rev Plant Biol, 2006, 57: 477–496. doi: 10.1146/annurev.arplant.57.032905.105320 16669771

3. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang, Z. Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell, 2005, 120: 687–700. doi: 10.1016/j.cell.2004.12.026 15766531

4. Scheres B, Wolkenfelt H. The Arabidopsis, root as a model to study plant development. Plant Physiol Bioch, 1998, 36:21–32.

5. Sampathkumar A, Yan A, Krupinski P, Meyerowitz EM. Physical forces regulate plant development and morphogenesis. Curr Biol, 2014, 24: R475–R483. doi: 10.1016/j.cub.2014.03.014 24845680

6. Sambade A, Findlay K, Schaffner AR, Meyerowitz E. Actin dependent and -independent functions of cortical microtubules in the differentiation of Arabidopsis leaf trichomes. Plant Cell, 2014, 26, 1629–1644. doi: 10.1105/tpc.113.118273 24714762

7. Luckwill L.C. The genus Lycopersicon: A historical, biological and taxonomic survey of the wild and cultivated tomato. Aberd Univ Stud, 1943, 120:1–44.

8. Fu Y. The cytoskeleton in the pollen tube. Curr Opin Plant Biol, 2015, 28:111–119. doi: 10.1016/j.pbi.2015.10.004 26550939

9. Li J, Wang X, Qin T, Zhang Y, Liu X, Sun J, et al. MDP25, a novel calcium regulatory protein, mediates hypocotyl cell elongation by destabilizing cortical microtubules in Arabidopsis. Plant Cell, 2011, 23:4411–4427. doi: 10.1105/tpc.111.092684 22209764

10. Galatis B, Apostolakos P. The Role of the cytoskeleton in the morphogenesis and function of stomatal complexes. New Phytol, 2010, 161:613–639.

11. Ren H, Dang X, Cai X, Yu P, Li Y, Zhang S, et al. Spatio-temporal orientation of microtubules controls conical cell shape in Arabidopsis thaliana petals. Plos Genet, 2017, 13(6): e1006851. doi: 10.1371/journal.pgen.1006851 28644898

12. Van BN, Joss G, Van OP. Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol, 2004, 136(4):3905–3919. doi: 10.1104/pp.103.031591 15557102

13. Baskin TI, Beemster GT, Judy-March JE, Marga F. Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis. Plant Physiol, 2004, 135:2279–2290. doi: 10.1104/pp.104.040493 15299138

14. Hepler PK, Vidali L, Cheung AY. Polarized cell growth in higher plants. Annu Rev Cell Dev Bi, 2001, 17:159–187.

15. Menand B, Calder G, Dolan L. Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens. J Exp Bot, 2007, 58:1843–1849. doi: 10.1093/jxb/erm047 17404383

16. Smith LG, Oppenheimer DG. Spatial control of cell expansion by the plant cytoskeleton. Annu rev cell Dev Bi. 2017, 21, 271–95.

17. Sheahan M.B, Staiger, CJ, Rose RJ, McCurdy DW. A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol, 2004, 136: 3968–3978. doi: 10.1104/pp.104.049411 15557099

18. Le J, El-Assal SE, Basu D, Saad ME, Szymanski DB. Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Curr Biol, 2003, 13: 1341–1347 doi: 10.1016/s0960-9822(03)00493-7 12906796

19. Kost B, Spielhofer P, Chua NH. A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J, 1998, 16: 393–401 doi: 10.1046/j.1365-313x.1998.00304.x 9881160

20. Vidali L, Rounds CM, Hepler PK, Bezanilla M. Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. Plos One, 2009, 4: e5744. doi: 10.1371/journal.pone.0005744 19478943

21. Zhang M, Zhang R, Qu X, Huang S. Arabidopsis FIM5 decorates apical actin filaments and regulates their organization in the pollen tube. J Exp Bot, 2016, 67(11):3407–3417. doi: 10.1093/jxb/erw160 27117336

22. Lovy-Wheeler A, Kunkel JG, Allwood EG, Hussey PJ, Hepler PK. Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily. Plant Cell, 2005, 18, 2182–2193.

23. Gu Y, Fu Y, Dowd P, Li S, Vernoud V, Gilroy S et al. A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol, 2005, 169(1):127–138. doi: 10.1083/jcb.200409140 15824136

24. Qu X, Zhang H, Xie Y, Wang J, Chen N, Huang S. Arabidopsis Villins promote actin turnover at pollen tube tips and facilitate the construction of actin collars. Plant Cell, 2013, 25: 1803–1817. doi: 10.1105/tpc.113.110940 23715472

25. Qu X, Zhang R, Zhang M, Diao M, Xue Y, Huang S. Organizational innovation of apical actin filaments drives rapid pollen tube growth and turning. Mol Plant, 2017(7): 930–947. doi: 10.1016/j.molp.2017.05.002 28502709

26. Basu D, Le J, El-Essal Sel D, Huang S, Zhang C, Mallery EL, et al. DISTORTED3/SCAR2 is a putative Arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis. Plant Cell, 2005, 17:502–24. doi: 10.1105/tpc.104.027987 15659634

27. Mathur J, Mathur N, Kernebeck B, Hülskamp M. Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell, 2003, 15:1632–45. doi: 10.1105/tpc.011676 12837952

28. Yanagisawa M, Desyatova AS, Belteton SA, Mallery EL, Turner JA, Szymanski DB. Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis. Nature Plants, 2015, 1(3):15014.

29. Folkers U, Kirik V, Schöbinger U, Falk S, Krishnakumar S, Pollock MA, et al. The cell morphogenesis gene ANGUSTIFOLIA encodes a CtBP/BARS-like protein and is involved in the control of the microtubule cytoskeleton. EMBO J, 2002, 21:1280–8. doi: 10.1093/emboj/21.6.1280 11889034

30. Oppenheimer DG, Pollock MA, Vacik J, Ericson B, Feldmann K, Marks MD. Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis. P Natl Acad Sci, 1997, 94:6261–6.

31. Torres-Ruiz RA, Jurgens G. Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development, 1994, 120:2967–78. 10484674

32. Yu Y, Wu S. Nowak J, Wang G, Han L, Feng Z, et al. Live-cell imaging of the cytoskeleton in elongating cotton fibres. Nat plants, 2019, 5, 498–504. doi: 10.1038/s41477-019-0418-8 31040442

33. Kang JH, Campos ML, Zemelis-Durfee S, Al-Haddad JM, Jones AD, Telewski FW, et al. Molecular cloning of the tomato Hairless gene implicates actin dynamics in trichome-mediated defense and mechanical properties of stem tissue. J Exp Bot, 2016, 67(18):5313–5324. doi: 10.1093/jxb/erw292 27481446

34. Szymanski DB. Breaking the WAVE complex: the point of Arabidopsis trichomes. Curr Opin Plant Biol, 2005, 8(1):103–112. doi: 10.1016/j.pbi.2004.11.004 15653407

35. Mathur J, Chua NH. Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. Plant Cell, 2000, 12, 465–477. doi: 10.1105/tpc.12.4.465 10760237

36. Zhang C, Mallery EL, Schlueter J, Huang S, Fan Y, Brankle S, et al. Arabidopsis SCARs function interchangeably to meet actin-related protein 2/3 activation thresholds during Morphogenesis. Plant Cell, 2008, 20:995. doi: 10.1105/tpc.107.055350 18424615

37. Jeong NR, Kim H, Hwang IT, Howe GA, Kang JH. Genetic analysis of the tomato inquieta mutant links the ARP2/3 complex to trichome development. J Plant Biol, 2017, 60(6):582–592.

38. Ren H, Dang X, Yang Y, Huang D, Liu M, Gao X, et al. SPIKE1 Activates ROP GTPase to modulate petal growth and shape. Plant Physiol, 2016, 172:358–371. doi: 10.1104/pp.16.00788 27440754

39. Fu Y, Li H, Yang Z. The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell, 2002, 14:777–94. doi: 10.1105/tpc.001537 11971134

40. Paredez AR, Somerville CR, Ehrhardt DW. Visualization of cellulose synthase demonstrates functional association with microtubules. Science, 2006, 312:1491–1495. doi: 10.1126/science.1126551 16627697

41. Zabotina O, Malm E, Drakakaki G. Identification and preliminary characterization of a new chemical affecting glucosyltransferase activities involved in plant cell wall biosynthesis. Mol Plant. 2008, 1:977–89. doi: 10.1093/mp/ssn055 19825597

42. Qi J, Wu B, Feng S, Lü S, Guan C, Zhang X, et al. Mechanical regulation of organ asymmetry in leaves. Nat Plants, 2017, 3:724–733. doi: 10.1038/s41477-017-0008-6 29150691

43. Smith LG. Cytoskeletal control of plant cell shape: getting the fine points. Curr Opin Plant Biol, 2003, 6:63–73. 12495753

44. Szymanski DB, Wick M. Organized F-Actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell, 1999, 11(12):2331–2347. doi: 10.1105/tpc.11.12.2331 10590162

45. Dong H, Pei W, Ren H. Actin fringe is correlated with tip growth velocity of pollen tubes. Mol Plant, 2012, 5:1160–1162. doi: 10.1093/mp/sss073 22863760

46. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, et al. Lifeact: a versatile marker to visualize F-actin. Nat Methods, 2008, 5:605–607. doi: 10.1038/nmeth.1220 18536722

47. Garcia V, Bres C, Just D, Fernandez L, Tai FW, Mauxion JP, et al. Rapid identification of causal mutations in tomato EMS populations via mapping-by-sequencing. Nat Protoc, 2016, 11:2401–18. doi: 10.1038/nprot.2016.143 27809315

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