Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12‐oxo‐phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection

Abstract

The moss Physcomitrella patens is an evolutionarily basal model system suitable for the analysis of plant defence responses activated after pathogen assault. Upon infection with the necrotroph Botrytis cinerea, several defence mechanisms are induced in P. patens, including the fortification of the plant cell wall by the incorporation of phenolic compounds and the induced expression of related genes. Botrytis cinerea infection also activates the accumulation of reactive oxygen species and cell death with hallmarks of programmed cell death in moss tissues. Salicylic acid (SA) levels also increase after fungal infection, and treatment with SA enhances transcript accumulation of the defence gene phenylalanine ammonia-lyase (PAL) in P. patens colonies. The expression levels of the genes involved in 12-oxo-phytodienoic acid (OPDA) synthesis, including lipoxygenase (LOX) and allene oxide synthase (AOS), increase in P. patens gametophytes after pathogen assault, together with a rise in free linolenic acid and OPDA concentrations. However, jasmonic acid (JA) could not be detected in healthy or infected tissues of this plant. Our results suggest that, although conserved defence signals, such as SA and OPDA, are synthesized and are probably involved in the defence response of P. patens against B. cinerea infection, JA production appears to be missing. Interestingly, P. patens responds to OPDA and methyl jasmonate by reducing moss colony growth and rhizoid length, suggesting that jasmonate perception is present in mosses. Thus, P. patens can provide clues with regard to the evolution of different defence pathways in plants, including signalling and perception of OPDA and jasmonates in nonflowering and flowering plants.

On plant defense signaling networks and early land plant evolution

“…In the moss Physcomitrella patens , papillae formation is readily observed close to unsuccessful infection attempts by different Phytophthora pathogens [61]. Oomycete and fungal pathogens also induce ROS [62,63] and inoculations with oomycetes resulted in the accumulation of toxic phenolic compounds in P. patens [61,62]. Similarly, other mosses, including Funaria hygrometrica , also form papillae around fungal penetration sites to prohibit their entry [64,65].…”

“…They also have been explored with regard to pathogen defense in non-flowering land plants. SA has been measured in mosses and gymnosperms – indeed, as in angiosperms, SA has been shown to accumulate in response to elicitors or pathogen attack [63,119,120], supporting its function in defense across land plant diversity.…”

“…Yet, when the moss P. patens was infected with two species of Pythium , an increase in the production of endogenous JA was detected over time and compared to control plants [62] – although the levels of JA were minimal both before and after infection. In contrast, exposure to the fungal pathogen Botrytis cinerea did not result in an increase in JA, but instead an increase in SA and the JA-precursor 12-oxo-phytodienoic acid (OPDA [63];). OPDA also increased after wounding in M. polymorpha [129].…”

“…In P. patens , infection by oomycete and fungal pathogens leads to up-regulation of the usual suspects of angiosperm defense signaling: PAL, Dirigent ( DIR ), Chalcone synthase ( CHS) and Pathogen related ( PR ) genes, as well as genes involved in JA and JA-precursor biosynthesis, such as LOX, AOS and OPR [62,63,137]. This is, however, not surprising, since infections with B. cinerea or two Pythium pathogens lead to OPDA production [62,63].…”

“…In P. patens , infection by oomycete and fungal pathogens leads to up-regulation of the usual suspects of angiosperm defense signaling: PAL, Dirigent ( DIR ), Chalcone synthase ( CHS) and Pathogen related ( PR ) genes, as well as genes involved in JA and JA-precursor biosynthesis, such as LOX, AOS and OPR [62,63,137]. This is, however, not surprising, since infections with B. cinerea or two Pythium pathogens lead to OPDA production [62,63]. In the spruce P. abies , the pathogens H. parviporum and H. annosum induce the expression of, among other genes, the JA biosynthesis and signaling genes LOX and Jasmonate Zim Domain ( JAZ ), as well as genes for the biosynthesis of ET ( ACO, 1-aminocyclopropane-1-carboxylic acid [ACC]-oxidase; ACS, ACC-synthase ), and PAL, DIR2/32 and PR1 [138-140].…”