measurements of plant tissue mechanics. Plant
Physiol 158:1514–1522
18. Majda M, Sapala A, Routier-Kierzkowska AL,
Smith RS (2019) Cellular force microscopy to
measure mechanical forces in plant cells. In:
Cvrc ˇkova ´ F, Z ˇ a ´rsky ´ V (eds) Plant cell morphogenesis. Methods in molecular biology, vol
1992. Humana, New York, p 285
19. Mosca G, Sapala A, Strauss S, RoutierKierzkowska AL, Smith RS (2017) On the
micro-indentation of plant cells in a tissue context. Phys Biol 14(1):015003
20. Peaucelle A, Braybrook SA, Le Guillou L,
Bron E, Kuhlemeier C, Ho ¨fte H (2011)
Pectin-induced changes in cell wall mechanics
underlie organ initiation in Arabidopsis. Curr
Biol 21:R840–R841
21. Beauzamy L, Derr J, Boudaoud A (2015)
Quantifying hydrostatic pressure in plant cells
by using indentation with an atomic force
microscope. Biophys J 108:2448–2456
22. Milani P, Gholamirad M, Traas J, Arne ´odo A,
Boudaoud A, Argoul F, Hamant O (2011) In
vivo analysis of local wall stiffness at the shoot
apical meristem in Arabidopsis using atomic
force microscopy. Plant J 67:1116–1123
23. Hutter JL, Bechhoefer J (1993) Calibration of
atomic-force microscope tips. Rev Sci Instrum
64:1868–1873
24. Maaloum M, Le ´vy R (2002) Measuring the
spring constant of atomic force microscope
cantilevers: thermal fluctuations and other
methods. Nanotechnology 33:33–37
25. Maivald P (1991) Using force modulation to
image surface elasticities with the atomic force
microscope. Nanotechnology 2:103–106
26. de Lange F, Cambi A, Huijbens R, de
Bakker B, Rensen W, Garcia-Parajo M, van
Hulst N, Figdor CG (2001) Cell biology
beyond the diffraction limit: near-field scanning optical microscopy. J Cell Sci
114:4153–4160
27. Chen Y, Cai J, Zhao T, Wang C, Dong S,
Luo S, Chen Z (2005) Atomic force microscopy imaging and 3-D reconstructions of serial
thin sections of a single cell and its interior
structures. Ultramicroscopy 103:173–182
28. Kirby AR (2011) Atomic force microscopy of
plant cell walls. In: Popper Z (ed) The plant cell
wall. Methods in molecular biology (methods
and protocols), vol 715. Humana Press,
Totowa, p 310
29. Wu JZ, Lin Y, Zhang XL, Pang DW, Zhao J
(2008) IAA stimulates pollen tube growth and
mediates the modification of its wall composition and structure in Torenia fournieri. J Exp
Bot 59:2529–2543
30. Wu Y, Wang S, Zhou D, Xing C, Zhang Y, Cai
Z (2010) Evaluation of elastic modulus and
hardness of crop stalks cell walls by nanoindentation.
Bioresour
Technol
101:2867–2871
31. Fernandes AN, Chen X, Scotchford CA,
Walker J, Wells DM et al (2012) Mechanical
properties of epidermal cells of whole living
roots of Arabidopsis thaliana: an atomic force
microscopy study. Phys Rev E Stat Nonlinear
Soft Matter Phys 85:021916
32. Radotic ´ K, Roduit C, Simonovic ´ J,
Hornitschek P, Fankhauser C et al (2012)
Atomic force microscopy stiffness tomography
on living Arabidopsis thaliana cells reveals the
mechanical properties of surface and deep cellwall layers during growth. Biophys J
103:386–394
33. Majda M, Grones P, Sintorn IM, Vain T, Milani
P et al (2017) Mechanochemical polarization
of contiguous cell walls shapes plant pavement
cells. Dev Cell 43:290–304
34. Kierzkowski D, Routier-Kierzkowska A (2019)
Cellular basis of growth in plants: geometry
matters. Curr Opin Plant Biol 47:56–63
35. Majda M, Krupinski P, Jo ¨nsson H, Hamant O,
Robert S (2019) Mechanical asymmetry of the
cell wall predicts changes in pavement cell
geometry. Dev Cell 50(1):9–10
36. Majda M (2019) Visualization of plant cell wall
epitopes using immunogold labeling for electron microscopy. Bio-protocol 9(7):e3205
37. Sambrook J, Fritsch EF, Maniatis T (1982)
Molecular cloning: a laboratory manual, 2nd
edn. Cold Spring Harbor Laboratory, Cold
Spring Harbor, p 2368
38. Foster B (2012) New atomic force microscopy
(AFM) approaches life sciences gently, quantitatively, and correctively. Am Lab 44:24–28
39. Derjaguin BV, Muller VM, Toporov Y (1975)
Effect of contact deformations on the adhesion
of particles. J Colloid Interface Sci 53:314–326
40. Fu Y, Li H, Yang Z (2002) The ROP2 GTPase
controls the formation of cortical fine F-actin
and the early phase of directional cell expansion
during Arabidopsis organogenesis. Plant Cell
14:777–794
Atomic Force Microscopy to Study Cell Wall Mechanics in Plants
369
Physiol 158:1514–1522
18. Majda M, Sapala A, Routier-Kierzkowska AL,
Smith RS (2019) Cellular force microscopy to
measure mechanical forces in plant cells. In:
Cvrc ˇkova ´ F, Z ˇ a ´rsky ´ V (eds) Plant cell morphogenesis. Methods in molecular biology, vol
1992. Humana, New York, p 285
19. Mosca G, Sapala A, Strauss S, RoutierKierzkowska AL, Smith RS (2017) On the
micro-indentation of plant cells in a tissue context. Phys Biol 14(1):015003
20. Peaucelle A, Braybrook SA, Le Guillou L,
Bron E, Kuhlemeier C, Ho ¨fte H (2011)
Pectin-induced changes in cell wall mechanics
underlie organ initiation in Arabidopsis. Curr
Biol 21:R840–R841
21. Beauzamy L, Derr J, Boudaoud A (2015)
Quantifying hydrostatic pressure in plant cells
by using indentation with an atomic force
microscope. Biophys J 108:2448–2456
22. Milani P, Gholamirad M, Traas J, Arne ´odo A,
Boudaoud A, Argoul F, Hamant O (2011) In
vivo analysis of local wall stiffness at the shoot
apical meristem in Arabidopsis using atomic
force microscopy. Plant J 67:1116–1123
23. Hutter JL, Bechhoefer J (1993) Calibration of
atomic-force microscope tips. Rev Sci Instrum
64:1868–1873
24. Maaloum M, Le ´vy R (2002) Measuring the
spring constant of atomic force microscope
cantilevers: thermal fluctuations and other
methods. Nanotechnology 33:33–37
25. Maivald P (1991) Using force modulation to
image surface elasticities with the atomic force
microscope. Nanotechnology 2:103–106
26. de Lange F, Cambi A, Huijbens R, de
Bakker B, Rensen W, Garcia-Parajo M, van
Hulst N, Figdor CG (2001) Cell biology
beyond the diffraction limit: near-field scanning optical microscopy. J Cell Sci
114:4153–4160
27. Chen Y, Cai J, Zhao T, Wang C, Dong S,
Luo S, Chen Z (2005) Atomic force microscopy imaging and 3-D reconstructions of serial
thin sections of a single cell and its interior
structures. Ultramicroscopy 103:173–182
28. Kirby AR (2011) Atomic force microscopy of
plant cell walls. In: Popper Z (ed) The plant cell
wall. Methods in molecular biology (methods
and protocols), vol 715. Humana Press,
Totowa, p 310
29. Wu JZ, Lin Y, Zhang XL, Pang DW, Zhao J
(2008) IAA stimulates pollen tube growth and
mediates the modification of its wall composition and structure in Torenia fournieri. J Exp
Bot 59:2529–2543
30. Wu Y, Wang S, Zhou D, Xing C, Zhang Y, Cai
Z (2010) Evaluation of elastic modulus and
hardness of crop stalks cell walls by nanoindentation.
Bioresour
Technol
101:2867–2871
31. Fernandes AN, Chen X, Scotchford CA,
Walker J, Wells DM et al (2012) Mechanical
properties of epidermal cells of whole living
roots of Arabidopsis thaliana: an atomic force
microscopy study. Phys Rev E Stat Nonlinear
Soft Matter Phys 85:021916
32. Radotic ´ K, Roduit C, Simonovic ´ J,
Hornitschek P, Fankhauser C et al (2012)
Atomic force microscopy stiffness tomography
on living Arabidopsis thaliana cells reveals the
mechanical properties of surface and deep cellwall layers during growth. Biophys J
103:386–394
33. Majda M, Grones P, Sintorn IM, Vain T, Milani
P et al (2017) Mechanochemical polarization
of contiguous cell walls shapes plant pavement
cells. Dev Cell 43:290–304
34. Kierzkowski D, Routier-Kierzkowska A (2019)
Cellular basis of growth in plants: geometry
matters. Curr Opin Plant Biol 47:56–63
35. Majda M, Krupinski P, Jo ¨nsson H, Hamant O,
Robert S (2019) Mechanical asymmetry of the
cell wall predicts changes in pavement cell
geometry. Dev Cell 50(1):9–10
36. Majda M (2019) Visualization of plant cell wall
epitopes using immunogold labeling for electron microscopy. Bio-protocol 9(7):e3205
37. Sambrook J, Fritsch EF, Maniatis T (1982)
Molecular cloning: a laboratory manual, 2nd
edn. Cold Spring Harbor Laboratory, Cold
Spring Harbor, p 2368
38. Foster B (2012) New atomic force microscopy
(AFM) approaches life sciences gently, quantitatively, and correctively. Am Lab 44:24–28
39. Derjaguin BV, Muller VM, Toporov Y (1975)
Effect of contact deformations on the adhesion
of particles. J Colloid Interface Sci 53:314–326
40. Fu Y, Li H, Yang Z (2002) The ROP2 GTPase
controls the formation of cortical fine F-actin
and the early phase of directional cell expansion
during Arabidopsis organogenesis. Plant Cell
14:777–794
Atomic Force Microscopy to Study Cell Wall Mechanics in Plants
369