Professional Documents
Culture Documents
One of the main differences between plant and animal cells biological processes such as cell morphogenesis as well as re-
are the walls surrounding plant cells providing structural sponse to both biotic and abiotic stresses (Landrein and
Plant Cell Physiol. 56(2): 215–223 (2015) doi:10.1093/pcp/pcu164, Advance Access publication on 21 November 2014,
available online at www.pcp.oxfordjournals.org
! The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
All rights reserved. For permissions, please email: journals.permissions@oup.com
T. Hamann | Concepts for plant cell wall integrity maintenance
Blaukopf 2010, Nühse 2012, Wolf et al. 2012, Engelsdorf and ligands, cell wall fragments and wall epitopes, which could be
Hamann 2014, Malinovsky et al. 2014, Wolf and Hofte 2014). involved in CWI maintenance by serving as indicators of the
While these reviews covered particular aspects such as recep- state of the wall. The latter possibilities are of particular interest
tor-like kinase (RLK)-based signaling processes and cell wall in plants since a large number of RLK-encoding genes have been
metabolism in the context of the plant CWI maintenance identified in plant genomes, with several of them implicated in
mechanism very thoroughly, the role of turgor pressure CWI maintenance (Engelsdorf and Hamann 2014).
during CWI maintenance has only been addressed to a limited In yeast, three different stimulus perception and signal gen-
extent. Therefore this review will try to assess the function of eration mechanisms are contributing to CWI maintenance and
turgor pressure in CWI maintenance and discuss different interact to different degrees (Fig. 1; Levin 2011). Stimulus de-
design possibilities for the mechanism. Information about the tection in the first one is mediated by a group of five plasma
S. cerevisiae CWI maintenance mechanism will be used initially membrane-localized proteins (WSC1–WSC3, MTL1 and MID2),
216
Plant Cell Physiol. 56(2): 215–223 (2015) doi:10.1093/pcp/pcu164
Signal translation from WSC1 to ROM1, a cytoplasmic, links between different signaling cascades perceiving CWS is
plasma membrane-associated guanosine nucleotide exchange the regulation of CCH1 activity by the previously mentioned
factor (GEF), is mediated via the small cytoplasmic domain in MAPK MPK1 (Rispail et al. 2009). Influx of Ca2+ ions into the
response to the previously mentioned conformational change cytoplasm activates yeast calmodulin, which in turn regulates
of the extracellular part of WSC1 (Levin 2011). ROM1 in turn the activity of calcineurin, a heterodimer that has Ca2+- and
mediates the GTP/GDP exchange at the small GTPase RHO1. calmodulin-dependent phosphatase activity. One of the pri-
RHO1 is a central integrator responding to different inputs, mary targets of calcineurin activity is CRZ1, a zinc finger tran-
whose activity is regulated both by GEFs (such asROM1/2 scription factor whose nuclear localization is dependent on
and TUS) and by GTPase-activating proteins (GAPs) dephosphorylation by calcineurin (Yoshimoto et al. 2002).
(Schmelzle et al. 2002, Yoshida et al. 2009). While ROM1 and Expression analysis has shown that CRZ1 regulates the activity
ROM2 are responsible for CWS-induced RHO1 activation, TUS of different P-ATPases involved in ion homeostasis and of FKS2,
217
T. Hamann | Concepts for plant cell wall integrity maintenance
effects allowing long-term modulated adaptations including glucose units organized in microfibrils that are produced by
changes in gene expression (around 500 transcript levels plasma membrane-localized rosette complexes (McFarlane
change within 10 min after initial stress perception) and inhib- et al. 2014). The composition of the rosette complexes active
ition of cell cycle progression (Capaldi et al. 2008). Interestingly, during primary cell wall formation differs from that of those
responses to hypo-osmotic stress lead primarily to transcript active during secondary cell wall formation, which also results
level changes in genes required for cell wall metabolism, while in different sensitivities to cellulose biosynthesis inhibitors such
hyperosmotic stress primarily affects genes required for glycerol as isoxaben (Heim et al. 1990). Isoxaben is a frequently used tool
and energy metabolism, hinting at qualitatively different re- in plant CWI maintenance research to cause CWS (Manfield
sponses required to adapt to hypo- vs. hyperosmotic stress. et al. 2004, Hematy et al. 2007, Hamann et al. 2009, Tsang et al.
To summarize, the available data from research into the 2011). It inhibits cellulose production during primary cell wall
yeast CWI maintenance mechanism show that three different formation by blocking the activity of CELLULOSE SYNTHASE A
218
Plant Cell Physiol. 56(2): 215–223 (2015) doi:10.1093/pcp/pcu164
219
T. Hamann | Concepts for plant cell wall integrity maintenance
resistance to different pathogens (Ralstonia solanacearum and plasma membrane in relation to the wall. From a turgor
Plectosphaerella cucumerina) compared with mutations in the point of view, this could correspond to a hypo-osmotic shock
genes required for primary cell wall formation (Hernandez- situation, with the available data supporting this view since
Blanco et al. 2007). This suggests that, for example, the patho- mild hyperosmotic shocks (support) suppress CWI impairment
gen infection mechanisms or the CWS responses could differ in Arabidopsis seedlings and yeast (Fig. 2; Hamann et al. 2009,
between elongating and differentiated cells and highlights the Levin 2011). In this scenario, stimuli would be perceived by
need for additional, detailed studies. (plasma membrane-localized) proteins, which are able to
sense displacement of the membrane vs. the wall (mechano-
sensitive) and/or changes in turgor pressure levels. Stimulus
Stimuli Indicating Cell Wall Integrity perception could lead to conformational changes (analogous
to WSC1) or opening of membrane channels (MID1–CCH1),
Impairment
220
Plant Cell Physiol. 56(2): 215–223 (2015) doi:10.1093/pcp/pcu164
MSLs and OSCA (Wilson et al. 2013, Kumar and Verslues 2014, Cano-Delgado, A.I., Metzlaff, K. and Bevan, M.W. (2000) The eli1 mutation
Yuan et al. 2014). reveals a link between cell expansion and secondary cell wall formation
in Arabidopsis thaliana. Development 127: 3395–3405.
To summarize, currently it is an exciting time to work on the
Capaldi, A.P., Kaplan, T., Liu, Y., Habib, N., Regev, A., Friedman, N. and
plant CWI maintenance mechanism since enough evidence has O’Shea, E.K. (2008) Structure and function of a transcriptional network
accumulated to support the notion that it is an important activated by the MAPK Hog1. Nat. Genet. 40: 1300–1306.
component of plant developmental, stress response and cell Cullen, P.J., Sabbagh, W., Graham, E., Irick, M.M., van Olden, E.K., Neal, C.
wall metabolic processes. Additionally the available functional et al. (2004) A signaling mucin at the head of the Cdc42- and MAPK-
data provide sufficient guidance for targeted, hypothesis-driven dependent filamentous growth pathway in yeast. Genes Dev. 18:
experiments to dissect its mode of action. In parallel it has been 1695–1708.
Denness, L., McKenna, J.F., Segonzac, C., Wormit, A., Madhou, P.,
suggested that understanding the mechanism may generate
Bennett, M. et al. (2011) Cell wall damage-induced lignin biosynthesis
novel options to overcome successfully the plasticity of plant
221
T. Hamann | Concepts for plant cell wall integrity maintenance
protein, is required for Ca2+ influx and mating. Mol. Cell. Biol. 14: Miedes, E., Vanholme, R., Boerjan, W. and Molina, A. (2014) The role of the
8259–8271. secondary cell wall in plant resistance to pathogens. Front. Plant Sci. 5:
Jendretzki, A., Wittland, J., Wilk, S., Straede, A. and Heinisch, J.J. (2011) How 1–13.
do I begin? Sensing extracellular stress to maintain yeast cell wall Monshausen, G.B. and Haswell, E.S. (2013) A force of nature: molecular
integrity. Eur. J. Cell Biol. 90: 740–744. mechanisms of mechanoperception in plants. J. Exp. Bot. 64: 4663–4680.
Jung, U.S. and Levin, D.E. (1999) Genome-wide analysis of gene expression Moura, J.C.M.S., Bonine, C.A.V., Viana, J.D.F., Dornelas, M.C. and
regulated by the yeast cell wall integrity signalling pathway. Mol. Mazzafera, P. (2010) Abiotic and biotic stresses and changes in the
Microbiol. 34: 1049–1057. lignin content and composition in plants. J. Integr. Plant Biol. 52:
Jung, U.S., Sobering, A.K., Romeo, M.J. and Levin, D.E. (2002) Regulation of 360–376.
the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP Nakayama, K., Nagasu, T., Shimma, Y., Kuromitsu, J. and Jigami, Y. (1992)
kinase. Mol. Microbiol. 46: 781–789. OCH1 encodes a novel membrane bound mannosyltransferase: outer
Kamada, Y., Jung, U.S., Piotrowski, J. and Levin, D.E. (1995) The protein chain elongation of asparagine-linked oligosaccharides. EMBO J. 11:
222
Plant Cell Physiol. 56(2): 215–223 (2015) doi:10.1093/pcp/pcu164
Seifert, G.J. and Blaukopf, C. (2010) Irritable walls: the plant extracellular Wang, Y., Chantreau, M., Sibout, R. and Hawkins, S. (2013) Plant cell wall
matrix and signaling. Plant Physiol. 153: 467–478. lignification and monolignol metabolism. Front. Plant Sci. 4: 220.
Sénéchal, F., Wattier, C., Rustérucci, C. and Pelloux, J. (2014) Wilson, M.E., Maksaev, G. and Haswell, E.S. (2013) MscS-like
Homogalacturonan-modifying enzymes: structure, expression, and mechanosensitive channels in plants and microbes. Biochemistry 52:
roles in plants. J. Exp. Bot. 65: 5125–5160. 5708–5722.
Shankarnarayan, S., Narang, S.S., Malone, C.L., Deschenes, R.J. and Wolf, S., Hématy, K. and Höfte, H. (2012) Growth control and cell wall
Fassler, J.S. (2008) Modulation of yeast Sln1 kinase activity by the signaling in plants. Annu. Rev. Plant Biol. 63: 381–407.
CCW12 cell wall protein. J. Biol. Chem. 283: 1962–1973. Wolf, S. and Hofte, H. (2014) Growth control: a saga of cell walls, ROS, and
Stolz, A., Riefler, M., Lomin, S.N., Achazi, K., Romanov, G.A. and peptide receptors. Plant Cell 26: 1848–1856.
Schmulling, T. (2011) The specificity of cytokinin signalling in Wolf, S., Rausch, T. and Greiner, S. (2009) The N-terminal pro region
Arabidopsis thaliana is mediated by differing ligand affinities and ex- mediates retention of unprocessed type-I PME in the Golgi apparatus.
pression profiles of the receptors. Plant J. 67: 157–168. Plant J. 58: 361–375.
223