From morphogenesis to pathogenesis: A cellulose loosening protein is one of the most widely distributed tools in nature

Abstract

31 Plants must rearrange the network of complex carbohydrates in their cell walls during normal 32 growth and development. To accomplish this, all plants depend on proteins called expansins that 33 non-enzymatically loosen hydrogen bonds between cellulose microfibrils. Because of their key 34 role in cell wall extension during growth, expansin genes are ubiquitous, diverse, and abundant 35 throughout all land plants. Surprisingly, expansin genes have more recently been found in some 36 bacteria and microbial eukaryotes, where their biological functions are largely unknown. Here, 37we reconstruct the phylogeny of microbial expansin genes. We find these genes in all eukaryotic 38 microorganisms that have structural cellulose in their cell walls, suggesting expansins evolved in 39 ancient marine microorganisms long before the evolution of land plants. We also find expansins 40 in an unexpectedly high phylogenetic diversity of bacteria and fungi that do not have cellulosic 41 cell walls. These bacteria and fungi with expansin genes inhabit varied ecological contexts 42 mirroring the diversity of terrestrial and aquatic niches where plant and/or algal cellulosic cell 43 walls are present.

A horizontally acquired expansin gene increases virulence of the emerging plant pathogenErwinia tracheiphila

“…, Dickeya spp. , Pantoea stewartii and E. tracheiphila ) comprise one group, and the expansin homologs from Xanthomonadaceae comprise a second group (8). Erwinia tracheiphila and Pantoea stewartii are the only species with microbial expansin homologs from the Erwinia and Pantoea genera, respectively.…”

“…Expansin-coding genes are ubiquitous in all species of land plants and green algae, where they fulfill the essential role of non-enzymatically loosening cell wall cellulose during normal growth of any rapidly expanding tissues (11, 14-18). In bacteria and fungi – which do not have cellulosic cell walls – expansin genes are variably present in species that interact with live or dead plant or algal matter (7, 8, 10, 19). The function(s) of expansins in microbes are unknown for almost all species, but are thought to promote colonization of plants through interactions with plant cell wall cellulose (7, 8, 20).…”

“…In bacteria and fungi – which do not have cellulosic cell walls – expansin genes are variably present in species that interact with live or dead plant or algal matter (7, 8, 10, 19). The function(s) of expansins in microbes are unknown for almost all species, but are thought to promote colonization of plants through interactions with plant cell wall cellulose (7, 8, 20).…”

“…In the bacterial plant pathogen Ralstonia solanacearum , an expansin deletion mutant has decreased virulence (24), and in Clavibacter michiganensis , studies have described contradictory expansin roles for virulence and ability to colonize xylem (24-28). Overall, fundamental questions surrounding how microbial expansins mediate plant colonization in divergent genetic backgrounds and variable ecological contexts, and the molecular mechanism(s) by which microbial expansins interact with plant structural carbohydrates remain enigmatic (7, 8, 10, 19, 20, 24, 26, 29, 30).…”

“…The bacterial plant pathogen Erwinia tracheiphila Smith (Enterobacteriaceae), the causative agent of bacterial wilt of cucurbits, contains an operon with an expansin gene ( exlx ) and a gene fragment with a glycoside hydrolase family 5 functional domain ( gh5 ) (8, 31-33). The only geographic region where E. tracheiphila occurs is temperate Eastern North America, and it only infects species in two genera of cucurbit host plants: summer and winter squash (cultivars of Cucurbita spp.)…”