Dynamic cell wall modifications in brassicas during clubroot disease

Abstract

15 Biotic interactions of plants and microbial pathogens can cause drastic changes in cell wall 16 composition in response to developmental reprogramming caused as consequence of an 17 infection. Clubroot disease, caused by the biotrophic plant pathogen Plasmodiophora brassicae 18 (Phytomyxea, Rhizaria), is the economically most important disease of Brassica crops 19 worldwide. The disease is best known by the characteristic hypertrophied roots (root galls, 20 clubroots). Amongst a series of physiological changes of the host tissue, the formation of the 21 characteristic root galls leads to cell wall modification and reorganization. Cell wall chemistry 22 and the hosts genetic repertoire are discussed to play a role in the resilience of plants against 23 clubroot disease. Plant cells infected with P. brassicae are markedly enlarged, and look very 24 differently from uninfected, healthy cells. Here we systematically review cell wall related 25 processes that lead to the typical clubroot phenotype and provide novel insights how P. 26 brassicae uses these modifications to benefit its own development. An infection with P. 27 brassicae impacts on nearly all cell wall related processes, but all alterations are meaningful for 28 successful growth and development of P. brassicae. Processes related to cell wall stability and 29 rigidity (e.g. cellulose, pectin or lignin synthesis) are down-regulated, while cell wall degrading 30 enzymes or processes that increase the flexibility of the host cell wall (e.g. expansin) are up-31 regulated. The here presented findings indicate that P. brassicae weakens the structural stability 32 of its host cell while it increases its elasticity, which in consequence allows P. brassicae to 33 grow bigger and ultimately to develop more resting spores. Consequently, the understanding of 34 the modification of the host cell wall is important for the formation of the characteristic root 35 galls but also to better understand clubroot disease.36 37

Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation

“…A general overview on the expression of genes whose products are involved in cell wall loosening or degradation during late stages of gall development in Arabidopsis shows that only a limited number of genes are induced and a large number of them are in fact downregulated ( Supplementary Figure S4 ). Recent work of Badstöber et al (2020) showed that a large number of PME gene transcripts increased in mature galls in P. brassicae -infected kohlrabi ( Brassica oleracea ). They also found increased expression of other genes whose products may be involved in cell expansion ( XTH or EXP ) or degradation ( GH9 cellulases ) processes.…”

“…These events have a vast impact on tensions at the organ level; therefore, regulation of cell wall dynamics involves appropriate control of the cell adhesion/cell separation balance that is highly dependent on pectin status, and secondary cell wall modifications ( Jarvis et al, 2003 ). Transcriptomic and proteomic studies of clubroot disease have identified extensive changes in host genes and proteins involved in cell wall synthesis and turnover ( Devos et al, 2006 ; Badstöber et al, 2020 ). Additionally, host cell wall degradation or thickening has been documented at the microscopic level ( Donald et al, 2008 ).…”

Multi-Omics Approaches to Improve Clubroot Resistance in Brassica with a Special Focus on Brassica oleracea L.

“…While pectin plays an important role in cell expansion, adhesion, strength, and porosity, lignification protects cell wall polysaccharides from degradation [ 253 ]. Down-regulation of genes involved in the biosynthesis of cellulose, hemicellulose, pectin, callose, and lignin decreased root cell wall rigidity and stability of the clubroot infected cells of Brassica plants [ 254 ]. On the contrary, enzymes responsible for degrading these elements were up-regulated in clubroots.…”

“…However, to protect the plant cells from excessive degradation from pectinase, host plants produce enzyme-inhibiting enzymes, such as PMEIs (PME-inhibitor) and PGIPs (PG-inhibiting protein). In the clubroots of Brassica plants, the genes coding these inhibitors were down-regulated [ 254 ]. Plant cell-wall-degrading enzymes (CWDEs) play an important role in loosening and the breakdown of cell wall components [ 255 ] and establishment of pathogens [ 256 ].…”

“…Conversely, PAL and other genes involved in lignin biosynthesis ( C4H, 4CL, COMT, CCR1, F5H ) were down-regulated in clubroot infected tissue of B . oleracea [ 254 ]. Guaiacyl and syringyl are the vital components of the cell wall of angiosperms [ 262 ], and six genes associated with peroxidase are involved in the biosynthesis of guaiacyl, and syringyl lignin were up-regulated in clubroot-resistant wild cabbage [ 183 ].…”