Obligate Biotroph Pathogens of the Genus Albugo Are Better Adapted to Active Host Defense Compared to Niche Competitors

Abstract

Recent research suggested that plants behave differently under combined versus single abiotic and biotic stress conditions in controlled environments. While this work has provided a glimpse into how plants might behave under complex natural conditions, it also highlights the need for field experiments using established model systems. In nature, diverse microbes colonize the phyllosphere of Arabidopsis thaliana, including the obligate biotroph oomycete genus Albugo, causal agent of the common disease white rust. Biotrophic, as well as hemibiotrophic plant pathogens are characterized by efficient suppression of host defense responses. Lab experiments have even shown that Albugo sp. can suppress non-host resistance, thereby enabling otherwise avirulent pathogen growth. We asked how a pathogen that is vitally dependent on a living host can compete in nature for limited niche space while paradoxically enabling colonization of its host plant for competitors? To address this question, we used a proteomics approach to identify differences and similarities between lab and field samples of Albugo sp.-infected and -uninfected A. thaliana plants. We could identify highly similar apoplastic proteomic profiles in both infected and uninfected plants. In wild plants, however, a broad range of defense-related proteins were detected in the apoplast regardless of infection status, while no or low levels of defense-related proteins were detected in lab samples. These results indicate that Albugo sp. do not strongly affect immune responses and leave distinct branches of the immune signaling network intact. To validate our findings and to get mechanistic insights, we tested a panel of A. thaliana mutant plants with induced or compromised immunity for susceptibility to different biotrophic pathogens. Our findings suggest that the biotroph pathogen Albugo selectively interferes with host defense under different environmental and competitive pressures to maintain its ecological niche dominance. Adaptation to host immune responses while maintaining a partially active host immunity seems advantageous against competitors. We suggest a model for future research that considers not only host–microbe but in addition microbe–microbe and microbe–host environment factors.

A Golgi-Released Subpopulation of the Trans-Golgi Network Mediates Protein Secretion in Arabidopsis

“…We noted that our dataset comprises a lower proportion of proteins with predicted peptides (;25%) than those in other studies (35% ; 50%). This lower proportion was likely due to differences in experimental procedures by which the apoplastic fluid was prepared-because a similar proportion (;29%) was recorded in another study based on a protocol similar to that applied in our study (Ruhe et al, 2016). Nonetheless, we reasoned that direct targets of the SYP4-VAMP721 pathway are highly likely to be transported from the ER through the Golgi apparatus and the GA-and GI-TGN, and thus we focused on proteins with predicted signal peptides ( Fig.…”

“…Apoplastic proteins were extracted as described in Ruhe et al (2016) with slight modifications. Briefly, 32-d-old Arabidopsis plants growing under shortday conditions (10 h light, 14 h dark) were inoculated with the Bgh K1 isolate and incubated for 0, 24, and 48 h under the same conditions.…”

The Defense Phytohormone Signaling Network Enables Rapid, High-Amplitude Transcriptional Reprogramming during Effector-Triggered Immunity

“…In each experiment, seven to nine biological replicates were obtained per genotype. DNA extraction was performed as described (Ruhe et al, 2016). The amounts of Hpa DNA and plant DNA were determined by quantitative PCR on the CFX Connect Real-Time PCR Detection System (Bio-Rad) using EvaGreen (Biotium).…”

Albugo candida race diversity, ploidy and host‐associated microbes revealed using DNA sequence capture on diseased plants in the field

“…Suppression of nonhost resistance by Albugo species is likely to be beneficial for some microorganisms (Agler et al ., ; Ruhe et al ., ), but it could also give an evolutionary advantage to the pathogen. For example, A. candida comprises at least 10 physiological races that have specialized on different Brassicaceae species (Hiura, ; Pound & Williams, ; Hill et al ., ; Kaur et al ., ; Meena et al ., ) including destructive pathogens of oilseed mustard ( B. juncea, Race 7), Brassica oleracea (Race 9), B. rapa (Race 2), radish ( Raphanus sativus, Race 1), and wild species ( Armoracia rusticana , Race 3; Capsella bursa‐pastoris , Race 4; Sisymbrium officinale, Race 5 and Rorippa islandica, Race 6).…”