Advertisement

Folding, Wrinkling, and Buckling in Plant Cell Walls

  • Dorota Borowska-Wykręt
  • Dorota Kwiatkowska
Chapter

Abstract

In this chapter, we discuss various cases of cell and tissue wrinkling or folding from the perspective of a putative mechanism of their formation—tissue folding in the contractile roots; cell or meristem surface folding in phyllotaxis generation; the formation of the stomata pore and various types of gas spaces; the development of jigsaw puzzle-shaped epidermal cells; and the wrinkling of cell wall layers after the removal of tensile stress. We also address the biological role of such shaped cells or tissues and the mechanical property or state of the cell wall or tissue that is manifested by its folding or wrinkling. Buckling and differential growth are likely ways to generate folds or wrinkles. The former is an intuitive mechanism from the mechanical perspective, while the latter derives from biology. Some cases of cell or tissue morphogenesis suggest that locally the two mechanisms may simultaneously contribute to the formation of a wavy shape.

Keywords

Aerenchyma Cell wall buckling Contractile roots Differential growth Intercalary gas spaces Leaf and petal epidermis Phyllotaxis 

Notes

Acknowledgements

Work in D.K. research team is supported by the National Science Centre, Poland, research grant MAESTRO no. 2011/02/A/NZ3/00079. We thank Dr. Agata Burian for the discussions and valuable comments on this manuscript and Dr. Magdalena Raczyńska-Szajgin for the micrographs of the A. grandiflora petal epidermis. The drawings presented in the figures were prepared using Adobe Design Premium CS4 (Adobe Systems Inc. USA) and CorelDRAW X6 (Corel Corp.).

References

  1. Abasolo WP, Yoshida M, Yamamoto H, Okuyama T (2009) Stress generation in aerial roots of Ficus elastica (Moraceae). IAWA J 30:216–224CrossRefGoogle Scholar
  2. Apostolakos P, Galatis B (1998) Probable involvement of cytoskeleton in stomatal-pore formation in Asplenium nidus L. Protoplasma 203:48–57CrossRefGoogle Scholar
  3. Apostolakos P, Galatis B (1999) Microtubule and actin filament organization during stomatal morphogenesis in the fern Asplenium nidus. II. Guard cells. New Phytol 141:209–223CrossRefGoogle Scholar
  4. Apostolakos P, Livanos P, Galatis B (2009) Microtubule involvement in the deposition of radial fibrillar callose arrays in stomata of the fern Asplenium nidus L. Cytoskeleton 66:342–349CrossRefGoogle Scholar
  5. Armour WJ, Barton DA, Law AMK, Overall RL (2015) Differential growth in periclinal and anticlinal walls during lobe formation in Arabidopsis cotyledon pavement cells. Plant Cell 27:2484–2500CrossRefPubMedPubMedCentralGoogle Scholar
  6. Augustine SM, Cherian AV, Syamaladevi DP, Subramonian N (2015) Erianthus arundinaceus HSP70 (EaHSP70) acts as a key regulator in the formation of anisotropic interdigitation in sugarcane (Saccharum spp. hybrid) in response to drought stress. Plant Cell Physiol 56:2368–2380CrossRefPubMedGoogle Scholar
  7. Baskin TI, Jensen OE (2013) On the role of stress anisotropy in the growth of stems. J Exp Bot 64:4697–4707CrossRefPubMedGoogle Scholar
  8. Beauzamy L, Louveaux M, Hamant O, Boudaoud A (2015) Mechanically, the shoot apical meristem of arabidopsis behaves like a shell inflated by a pressure of about 1 MPa. Front Plant Sci 6:1038CrossRefPubMedPubMedCentralGoogle Scholar
  9. Burian A, Ludynia M, Uyttewaal M, Traas J, Boudaoud A, Hamant O, Kwiatkowska D (2013) A correlative microscopy approach relates microtubule behaviour, local organ geometry and cell growth at the Arabidopsis shoot apical meristem. J Exp Bot 64:5753–5767CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bünning E, Biegert F (1953) Die Bildung der Spaltöffnungsinitialen bei Allium cepa. Z Bot 41:17–39Google Scholar
  11. Campbell R (1972) Electron microscopy of the development of needles of Pinus nigra var. maritima. Ann Bot 36:711–720CrossRefGoogle Scholar
  12. Chen X, Yin J (2010) Buckling patterns of thin films on curved compliant substrates with applications to morphogenesis and three-dimensional micro-fabrication. Soft Matter 6:5667–5680CrossRefGoogle Scholar
  13. Coen E, Rolland-Lagan A-G, Matthews M, Bangham JA, Prusinkiewicz P (2004) The genetics of geometry. Proc Natl Acad Sci USA 101:4728–4735CrossRefPubMedGoogle Scholar
  14. Cosgrove DJ (2016) Catalysts of plant cell wall loosening [version1; referees: 2 approved]. F1000Research, 5:F1000 Faculty Rev-119Google Scholar
  15. Cresswell A, Sackville Hamilton NR, Thomas H, Charnock RB, Cookson AR, Thomas BJ (1999) Evidence for root contraction in white clover (Trifolium repens L.). Ann Bot 84:359–369CrossRefGoogle Scholar
  16. Cyr RJ, Lin B-L, Jernstedt JA (1988) Root contraction in hyacinth. II. Changes in tubulin levels, microtubule number and orientation associated with differential cell expansion. Planta 174:446–452CrossRefPubMedGoogle Scholar
  17. Dumais J, Serikawa K, Mandoli DF (2000) Acetabularia: a unicellular model for understanding subcellular localization and morphogenesis during development. J Plant Growth Regul 19:253–264CrossRefGoogle Scholar
  18. Dumais J, Harrison L (2000) Whorl morphogenesis in the dasycladalean algae: the pattern formation viewpoint. Phil Trans R Soc Lond B 355:281–305CrossRefGoogle Scholar
  19. Dumais J, Steele ChR (2000) New evidence for role of mechanical forces in the shoot apical meristem. J Plant Growth Regul 19:7–18CrossRefGoogle Scholar
  20. Elsner J, Michalski M, Kwiatkowska D (2012) Spatiotemporal variation of leaf epidermal cell growth: a quantitative analysis of Arabidopsis thaliana wild-type and triple cyclinD3 mutant plants. Ann Bot 109:897–910CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fisher JB (2008) Anatomy of axis contraction in seedlings from a fire prone habitat. Am J Bot 95:1337–1348CrossRefPubMedGoogle Scholar
  22. Frank MJ, Smith LG (2002) A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr Biol 12:849–853CrossRefPubMedGoogle Scholar
  23. Fujita M, Himmelspach R, Ward J, Whittington A, Hasenbein N, Liu Ch, Truong TT, Galway ME, Mansfield SD, Hocart ChH, Wasteneys GO (2013) The anisotropy1 D604 N mutation in the Arabidopsis cellulose synthase1 catalytic domain reduces cell wall crystallinity and the velocity of cellulose synthase complexes. Plant Physiol 162:74–85CrossRefPubMedPubMedCentralGoogle Scholar
  24. Galatis B (1980) Microtubules and guard-cell morphogenesis in Zea mays L. J Cell Sci 45:211–244PubMedGoogle Scholar
  25. Galatis B, Mitrakos K (1980) The ultrastructural cytology of the differentiating guard cells of Vigna sinensis. Am J Bot 67:1243–1261CrossRefGoogle Scholar
  26. Galatis B, Apostolakos P (1991) Microtubule organization and morphogenesis of stomata in caffeine-affected seedlings of Zea mays. Protoplasma 165:11–26CrossRefGoogle Scholar
  27. Galatis B, Apostolakos P (2004) The role of the cytoskeleton in the morphogenesis and function of stomatal complexes. New Phytol 161:613–639CrossRefGoogle Scholar
  28. Gambles RL, Dengler RE (1982a) The anatomy of the leaf of red pine, Pinus resinosa. I. Nonvascular tissues. Can J Bot 60:2788–2803CrossRefGoogle Scholar
  29. Gambles RL, Dengler RE (1982b) The anatomy of the leaf of red pine, Pinus resinosa. II. Vascular tissues. Can J Bot 60:2804–2824CrossRefGoogle Scholar
  30. Geitmann A, Ortega JKE (2009) Mechanics and modelling of plant cell growth. Trends Plant Sci 14:467–478CrossRefPubMedGoogle Scholar
  31. Giannoutsou E, Sotiriou P, Apostolakos P, Galatis B (2013) Early local differentiation of cell wall matrix defines the contact sites in lobed mesophyll cells of Zea mays. Ann Bot 112:1067–1081CrossRefPubMedPubMedCentralGoogle Scholar
  32. Gough HJ, Elam CF, de Bruyne NA (1940) The stabilization of a thin sheet by a continuous supporting medium. J R Aeronaut Soc 44:12–43CrossRefGoogle Scholar
  33. Green PB (1999) Expression of pattern in plants: combining molecular and calculus-based biophysical paradigms. Am J Bot 86:1059–1076CrossRefGoogle Scholar
  34. Green PB, Steele CS, Rennich SC (1996) Phyllotactic patterns: a biophysical mechanism for their origin. Ann Bot 77:515–527CrossRefGoogle Scholar
  35. Hamant O, Moulia B (2016) How do plants read their own shapes? New Phytol 212:333–337CrossRefPubMedGoogle Scholar
  36. Harris WM (1971) Ultrastructural observations on the mesophyll cells of pine leaves. Can J Bot 49:1107–1109CrossRefGoogle Scholar
  37. Harrison LG, Snell J, Verdi R, Vogt DE, Zeiss GD, Green BR (1981) Hair morphogenesis in Acetabularia mediterranea: temperature-dependent spacing and models of morphogen waves. Protoplasma 106:211–221CrossRefGoogle Scholar
  38. Harrison LG, von Aderkas P (2004) Spatially quantitative control of the number of cotyledons in a clonal population of somatic embryos of hybrid larch Larix x leptoeuropaea. Ann Bot 93:423–434CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hejnowicz Z (2011) Plants as mechano-osmotic transducers. In: Wojtaszek P (ed) Mechanical integration of plant cells and plants. Springer, Berlin, Heidelberg, pp p241–p267CrossRefGoogle Scholar
  40. Hejnowicz Z, Barthlott W (2005) Structural and mechanical peculiarities of the petioles of giant leaves of Amorphophallus (Araceae). Am J Bot 92:391–403CrossRefPubMedGoogle Scholar
  41. Hejnowicz Z, Borowska-Wykręt D (2005) Buckling of inner cell wall layers after manipulations to reduce tensile stress: observations and interpretations for stress transmission. Planta 220:465–473CrossRefPubMedGoogle Scholar
  42. Hejnowicz Z, Sievers A (1996) Tissue stresses in organs of herbaceous plants. III. Elastic properties of the tissues of sunflower hypocotyl and origin of tissue stresses. J Exp Bot 47:519–528CrossRefGoogle Scholar
  43. Higaki T, Takigawa-Imamura H, Akita K, Kutsuna N, Kobayashi R, Hasezawa S, Miura T (2016) Exogenous cellulose switches cell interdigitation to cell elongation in an RIC1-dependent manner in Arabidopsis thaliana cotyledon pavement cells. Plant Cell Physiol 58:106–119Google Scholar
  44. Hiller GH (1872) Untersuchungen über die Epidermis der Blüthenblätter. Jahrb f wiss Bot 15:411–452Google Scholar
  45. Hoss S, Wernicke W (1995) Microtubules and the establishment of apparent cell wall invaginations in mesophyll cells of Pinus silvestris L. J Plant Physiol 147:474–476CrossRefGoogle Scholar
  46. Jarvis MC (1998) Intercellular separation forces generated by intracellular pressure. Plant Cell Environ 21:1307–1310CrossRefGoogle Scholar
  47. Jeffree CE, Dale JE, Fry SC (1986) The genesis of intercellular spaces in developing leaves of Phaseolus vulgaris L. Protoplasma 132:90–98CrossRefGoogle Scholar
  48. Jung G, Wernicke W (1990) Cell shaping and microtubules in developing mesophyll of wheat (Triticum aestivum L). Protoplasma 153:141–148CrossRefGoogle Scholar
  49. Kennaway R, Coen E, Green A, Bangham A (2011) Generation of diverse biological forms through combinatorial interactions between tissue polarity and growth. PLoS Comput Biol 7:e1002071CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kollöffel C, Linssen PW (1984) The formation of intercellular spaces in the cotyledons of developing and germinating pea seeds. Protoplasma 120:12–19CrossRefGoogle Scholar
  51. Kaufman PB, Petering LB, Yocum CS, Baic D (1970) Ultrastructural studies on stomata development in internodes of Avena sativa. Am J Bot 57:33–49CrossRefGoogle Scholar
  52. Kaul RB (1971) Diaphragms and aerenchyma in Scirpus validus. Am J Bot 58:808–816CrossRefGoogle Scholar
  53. Kay QON, Daoud HS, Stirton CH (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Lin Soc 83:57–84CrossRefGoogle Scholar
  54. Kotzer AM, Wasteneys GO (2006) Mechanisms behind the puzzle: microtubule-microfilament cross-talk in pavement cell formation. Can J Bot 84:594–603CrossRefGoogle Scholar
  55. Liang F, Shen L-Z, Chen M, Yang Q (2008) Formation of intercellular gas space in the diaphragm during the development of aerenchyma in the leaf petiole of Sagittaria trifolia. Aqu Bot 88:185–195CrossRefGoogle Scholar
  56. Martynov LA (1975) A morphogenetic mechanism involving instability of initial form. J Theor Biol 52:471–480CrossRefPubMedGoogle Scholar
  57. Moose SP, Sisco PH (1994) Glossy15 controls the epidermal juvenile-to-adult phase transition in maize. Plant Cell 6:1343–1355CrossRefPubMedPubMedCentralGoogle Scholar
  58. Niklas KJ, Paolillo DJ (1998) Preferential states of longitudinal tension in the outer tissues of Taraxacum officinale (Asteraceae) peduncles. Am J Bot 85:1068–1081CrossRefPubMedGoogle Scholar
  59. Palevitz BA, Hepler PK (1976) Cellulose microfibril orientation and cell shaping in developing guard cells of Allium: the role of microtubules and ion accumulation. Planta 132:71–93CrossRefPubMedGoogle Scholar
  60. Panteris E, Apostolakos P, Galatis B (1993a) Microtubule organization, mesophyll cell morphogenesis and intercellular space formation in Adiantum capillus-veneris leaflets. Protoplasma 172:97–110CrossRefGoogle Scholar
  61. Panteris E, Apostolakos P, Galatis B (1993b) Microtubule organization and cell morphogenesis in two semi-lobed cell types of Adiantum capillus-veneris L. leaflets. New Phytol 125:509–520CrossRefGoogle Scholar
  62. Panteris E, Apostolakos P, Galatis B (1994) Sinuous ordinary epidermal cells: behind several patterns of waviness, a common morphogenetic mechanism. New Phytol 127:771–780CrossRefGoogle Scholar
  63. Parker ChC, Parker ML, Smith AC, Waldron KW (2001) Pectin distribution at the surface of potato parenchyma cells in relation to cell-cell adhesion. J Agric Food Chem 49:4364–4371CrossRefPubMedGoogle Scholar
  64. Prat R, André JP, Mutaftschiev S, Catesson AM (1997) Three-dimensional study of the intercellular gas space in Vigna radiate hypocotyl. Protoplasma 196:69–77Google Scholar
  65. Pütz N (1992) Measurement of the pulling force of a single contractile root. Can J Bot 70:1433–1439CrossRefGoogle Scholar
  66. Quintana A, Albrechtová J, Griesbach RJ, Freyre R (2007) Anatomical and biochemical studies of anthocyanidins in flowers of Anagallis monelli L. (Primulaceae) hybrids. Sci Hort 112:413–421CrossRefGoogle Scholar
  67. Raven JA (1996) Into the voids: the distribution, function, development and maintenance of gas spaces in plants. Ann Bot 78:137–142CrossRefGoogle Scholar
  68. Roland JC (1978) Cell wall differentiation and stages involved with intercellular gas space opening. J Cell Sci 32:325–336PubMedGoogle Scholar
  69. Romberger JA, Hejnowicz Z, Hill JF (1993) Plant structure: function and development. Springer, BerlinCrossRefGoogle Scholar
  70. Sack FD, Paolillo DJ Jr (1983a) Stomatal pore and cuticle formation in Funaria. Protoplasma 116:1–13CrossRefGoogle Scholar
  71. Sack FD, Paolillo DJ Jr (1983b) Structure and development of walls in Funaria stomata. Am J Bot 70:1019–1030CrossRefGoogle Scholar
  72. Sack FD (1987) The development and structure of stomata. In: Zeiger E, Farquhar GD, Cowan IR (eds) Stomatal function. Stanford University Press, Stanford, pp p59–p89Google Scholar
  73. Sampathkumar A, Krupiński P, Wightman R, Milani P, Berquand A, Boudaoud A, Hamant O, Jönsson H, Meyerowitz EM (2014) Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife 3:e01967Google Scholar
  74. Schreiber N, Gierlinger N, Putz N, Fratzl P, Neinhuis Ch, Burgert I (2010) G-fibres in storage roots of Trifolium pratense (Fabaceae): tensile stress generators for contraction. Plant J 61:854–861CrossRefPubMedGoogle Scholar
  75. Sego JL Jr, Marsh LC, Stevens KJ, Soukup A, Votrubová O, Enstone DE (2005) A re-examination of the root cortex on wetland flowering plants with respect to aerenchyma. Ann Bot 96:565–579CrossRefGoogle Scholar
  76. Sharon E, Efrati E (2010) The mechanics of non-Euclidean plates. Soft Matter 6:5693–5704CrossRefGoogle Scholar
  77. Sifton HB (1945) Air-space tissue in plants. Bot Rev 11:108–143CrossRefGoogle Scholar
  78. Singh AP, Srivastava LM (1973) The fine structure of pea stomata. Protoplasma 76:61–82CrossRefGoogle Scholar
  79. Smith-Huerta NL, Jernstedt JA (1989) Root contraction in hyacinth III. Orientation of cortical microtubules visualized by immunofluorescence microscopy. Protoplasma 151:1–10CrossRefGoogle Scholar
  80. Smith-Huerta NL, Jernstedt JA (1990) Root contraction in hyacinth IV. Orientation of cellulose microfibrils in radial longitudinal and transverse cell walls. Protoplasma 154:161–171CrossRefGoogle Scholar
  81. Sotiriou P, Giannoutsou E, Panteris E, Apostolakos P, Galatis B (2016) Cell wall matrix polysaccharide distribution and cortical microtubule organization: two factors controlling mesophyll cell morphogenesis in land plants. Ann Bot 117:401–419CrossRefPubMedPubMedCentralGoogle Scholar
  82. Srivastava LM, Singh AP (1972) Stomatal structure in corn leaves. J Ultrastruct Res 39:345–363CrossRefPubMedGoogle Scholar
  83. Staff L, Hurd P, Reale L, Seoighe C, Rockwood A, Gehring C (2012) The hidden geometries of the Arabidopsis thaliana epidermis. PLoS ONE 7:e43546CrossRefPubMedPubMedCentralGoogle Scholar
  84. Stebbins GL, Jain SK (1960) Developmental studies of cell differentiation in the epidermis of monocotyledons. I. Allium, Rhoeo and Commelina. Dev Biol 2:409–426CrossRefGoogle Scholar
  85. Stebbins GL, Shan SS (1960) Development studies of cell differentiation in the epidermis of monocotyledons. II. Cytological features of stomatal development in the Graminae. Dev Biol 2:477–500CrossRefGoogle Scholar
  86. Sylvester AW, Smith LG (2009) Cell biology of maize leaf development. In: Bennetzen JL, Hake SC (eds) Handbook of maize: its biology. Springer, New York, pp p179–p203CrossRefGoogle Scholar
  87. Szymanski DB (2014) The kinematics and mechanics of leaf expansion: new pieces to the Arabidopsis puzzle. Curr Opin Plant Biol 22:141–148CrossRefPubMedGoogle Scholar
  88. Tomlinson PB, Magellan TM, Griffith MP (2014) Root contraction in Cycas and Zamia (Cycadales) determined by gelatinous fibers. Am J Bot 101:1275–1285CrossRefPubMedGoogle Scholar
  89. Tsabary G, Shani Z, Roiz L, Levy I, Riov J, Shoseyov O (2003) Abnormal ‘wrinkled’ cell walls and retarded development of transgenic Arabidopsis thaliana plants expressing endo-1, 4-β-glucanase (cel1) antisense. Plant Mol Biol 51:213–224CrossRefPubMedGoogle Scholar
  90. Ugural AC (1999) Stresses in plates and shells. WCD McGraw-Hill, Boston-TorontoGoogle Scholar
  91. Urbanowicz BR, Bennett AB, del Campillo E, Catalá C, Hayashi T, Henrissat B, Höfte H, McQueen-Mason SJ, Patterson SE, Shoseyov O, Teeri TT, Rose JKC (2007) Structural organization and a standardized nomenclature for plant endo-1, 4-β-glucanases (cellulases) of glycosyl hydrolase family 9. Plant Physiol 144:1693–1696CrossRefPubMedPubMedCentralGoogle Scholar
  92. Wernicke W, Günther P, Jung G (1993) Microtubules and cell shaping in the mesophyll of Nigella damascena L. Protoplasma 173:8–12CrossRefGoogle Scholar
  93. Weston GD, Cass DD (1973) Observations on the development of the paraveinal mesophyll of soybean leaves. Bot Gaz 134:332–335CrossRefGoogle Scholar
  94. Wiebe HH, Al-Saadi HA (1976) The role of invaginations in armed mesophyll cells of pine needles. New Phytol 77:773–775CrossRefGoogle Scholar
  95. Yin J, Cao Z, Li C, Sheinman I, Chen X (2008) Stress-driven buckling patterns in spheroidal core/shell structures. P Natl Acad Sci USA 105:19132–19135CrossRefGoogle Scholar
  96. Zamski E, Ucko O, Koller D (1983) The mechanism of root contraction in Gymnarrhena micranatha, a desert plant. New Phytol 95:29–35CrossRefGoogle Scholar
  97. Zhang C, Halsey LE, Szymanski DB (2011) The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells. BMC Plant Biol 11:27CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of Biology and Environment Protection, Department of Biophysics and Morphogenesis of PlantsUniversity of Silesia in KatowiceKatowicePoland

Personalised recommendations