Plant cell wall integrity maintenance in model plants and crop species-relevant cell wall components and underlying guiding principles

Abstract

The walls surrounding the cells of all land-based plants provide mechanical support essential for growth and development as well as protection from adverse environmental conditions like biotic and abiotic stress. Composition and structure of plant cell walls can differ markedly between cell types, developmental stages and species. This implies that wall composition and structure are actively modified during biological processes and in response to specific functional requirements. Despite extensive research in the area, our understanding of the regulatory processes controlling active and adaptive modifications of cell wall composition and structure is still limited. One of these regulatory processes is the cell wall integrity maintenance mechanism, which monitors and maintains the functional integrity of the plant cell wall during development and interaction with environment. It is an important element in plant pathogen interaction and cell wall plasticity, which seems at least partially responsible for the limited success that targeted manipulation of cell wall metabolism has achieved so far. Here, we provide an overview of the cell wall polysaccharides forming the bulk of plant cell walls in both monocotyledonous and dicotyledonous plants and the effects their impairment can have. We summarize our current knowledge regarding the cell wall integrity maintenance mechanism and discuss that it could be responsible for several of the mutant phenotypes observed.

Keywords: Cell wall polysaccharides; Plant cell wall metabolism; Plant cell wall signaling; Plant defense; Plant environment interaction.

Fig. 1

Global overview of proteins mediating primary (PCW) and secondary cell wall (SCW) formation in dicots (Arabidopsis) and monocots (Oryza). Demonstrated or putative (indicated by ?) protein localizations are displayed in panel a based on data mostly derived from Arabidopsis. Enzymes such as PMEIs, PAEs and PMEs, which have been found in the apoplast, are listed outside the cells in panels a and b. Ellipses represent Golgi bodies/stacks with enzymes located to highlight their positions either inside the Golgi or associated with Golgi membranes. Circles containing enzymes like GALS1/2/3 or CTL1 represent Golgi-derived vesicles. Grey, dashed circles near the nucleus (black ellipse) represent the endoplasmic reticulum. b Summarizes putative localizations of proteins in Oryza. Abbreviations are explained in main text. Protein localizations are based on the following references: [, , , , , , , , , , , , , , , , , , , –270]

Fig. 2

Overview of CWI signaling components, their interactions and coordination between CWI and PTI signaling. Mechanical distortion of the CW induces CWI responses through THE1 and leads to production of elicitor peptides PEP1 and PEP3, which can suppress CWI responses and growth via PEPR1/2 (represented here by PEPR1) [198]. In parallel to mechanical distortion, the action of THE1 can be regulated by RALF34, which binds to THE1 at high apoplastic pH, leading to further alkalinisation of the apoplast [233]. THE1 activates CWI responses via MCA1 and FEI2 and NIA1 NIA2-dependent processes, which repress growth actively [198]. RALF1 and RALF23 induce alkalinization of the apoplast in a FER-dependent manner [247, 250]. Both of them also affect hormone signaling pathways through FER: RALF23 by inhibiting the de-stabilizing effect of FER on the transcription factor MYC2, a master regulator of JA signaling; RALF1 by activating ABI2, a repressor of ABA signaling [–249]. In addition, RALF23 has been shown to inhibit FER’s scaffold activity for pattern-recognition receptors (PRR) and their co-receptor BAK1, thus reducing sensitivity of the plant to respective PAMPs [232]. In addition to being involved in chemical signaling through PAMPs, RALFs and phytohormones, FER is capable of sensing physical signals from the CW, possibly through LRX proteins linking FER to CW [234]. Brown bars represents the cell wall (CW), grey bars represent the plasma membrane (PM). The white space in between the CW and PM represents the CW–PM interphase, where solutes can diffuse freely and changes in the mechanical forces are being sensed. Abbreviations are explained in main text