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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
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
Phagocytosis is a complex multi-gene trait of eukaryotes and allegedly one of the very defining features of this group. Although well documented for free-living unicellular eukaryotes and in specific cellular types of animals, data on phagocytosis in intracellular biotrophic parasites are scant. Indeed, the definition of intracellular biotrophy as complete reliance of a parasite on a living host, with which it constantly negotiates for the exchange of nutrients, is at odd with the consumption of particulate matter suggested by phagocytosis. Phytomyxea are intracellular biotrophic parasites infecting a broad group of hosts, ranging from plants to stramenopiles. They belong to the clade Rhizaria, where phagotrophy (i.e., phagocytosis as main mode to acquire nutrients) is the main mode of nutrition. The exact mode of nutrition of the biotrophic phytomyxea, including the agriculturally impactful phytomyxid Plasmodiophora brassicae, is still unresolved; despite investigations and the availability of molecular data. For other Phytomyxea, observations are patchy and molecular data altogether lacking. Here, using available genomic and transcriptomic data for Phytomyxea and the de novo sequenced transcriptome of the brown algae parasite Maullinia ectocarpii, we investigate the likelihood that the genetic machinery underpinning phagotrophy is conserved within the clade. We further document intracellular phagocytosis in P. brassicae and M. ectocarpii by transmission electron microscopy and fluorescent in situ hybridization. Our investigations confirm that molecular signatures underpinning phagocytosis exist in Phytomyxea and hint at a smaller subset of genes used for intracellular phagocytosis, which is similar between the two parasites. Microscopic evidence confirms the existence of intracellular phagocytosis, which seems to coexist with the manipulation of host physiology typical of biotrophic interactions. In both phytomyxid parasites investigated intracellular phagocytosis has adapted to the intracellular environment and seemingly targets specific organelles. Our findings shed light on the feeding behaviour of Phytomyxea, providing new molecular data for the class; and suggest a paramount and previously unrecognised role for phagocytosis in biotrophic interactions between host and parasite.
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