Plant Signals Anticipate the Induction of the Type III Secretion System in Pseudomonas syringae pv.
actinidiae
, Facilitating Efficient Temperature-Dependent Effector Translocation
Abstract:Plant diseases—their occurrence and severity—result from the impact of three factors: the host, the pathogen, and the environmental conditions, interconnected in the disease triangle. Time was further included as a fourth factor accounting for plant disease, leading to a more realistic three-dimensional disease pyramid to represent the evolution of disease over time.
“…Regarding P. syringae pv. actinidiae , our results confirmed a low-temperature dependency for T3SS efficiency (Puttilli et al ., 2022), which is entirely in line with the environmental conditions – in late winter or early spring – under which P. syringae pv. actinidiae is reported to cause disease or damage in the kiwifruit orchards (Kim et al ., 2017; Donati et al ., 2020).…”
Section: Discussionsupporting
confidence: 91%
“…glycinea could be involved in the regulation of T3SS-related gene expression in response to temperature (Ullrich et al ., 1995). Alternatively, if evidence hints that gene expression is not directly modified by temperature (Puttilli et al ., 2022), thermoregulation might act later in the transcription/translation chain, during T3SS assembly, or on translocation efficiency. In addition, the study of potential differences in membrane fluidity between strains is promising.…”
Section: Discussionmentioning
confidence: 99%
“…For each technical replicate, the conductivity value from the first measure was subtracted to values measured at each successive time points for normalization (Puttilli et al ., 2022). For each strain-temperature modality within each replicated experiment, conductivity was calculated as the average of the values of the three technical replicates for each time point, and ion-leakage curves over time were established accordingly.…”
Section: Methodsmentioning
confidence: 99%
“…On the other hand, for P. syringae pv. actinidiae strains, it was shown that there was no difference in hrpA1 promoter activity in vitro across a temperature range of 18-28°C, nonetheless, substantial differences were evident at a functional level, demonstrating a low-temperature dependency for T3SS efficiency for these strains (Puttilli et al ., 2022). However, the complete implications of warm temperatures on P. syringae virulence in plants remain poorly understood (Li et al ., 2006; Hockett et al ., 2013).…”
ThePseudomonas syringaespecies complex is a very important plant pathogenic bacterium, causing damage and economic losses on many crops. Research efforts for the understanding of the determinants of the host-range of a given strain are considerable. Recently, we showed that the inability of aP. syringaepv.actinidiaestrain to trigger ETI inA. thalianais due to an inefficient T3SS and not to the absence of a recognized effector. In this context, we compared severalP. syringaestrains belonging to different phylogroups and carrying the same plasmid-born avirulence gene for their ability to induce an HR inA. thalianaCol-0, as a marker of T3SS efficiency.PtoDC3000AvrBandPmaM6AvrBconsistently triggered a strong HR while other strains induced it at different intensities significantly depending on temperature. Both behaviors of low and warm temperature-dependency for T3SS efficiency were observed among thermosensitive strains, irrespective of theirin-vitrogrowth optimum. Surprisingly, differences were also observed among quasi-clonal strains. These results reveal a strongly strain-specific regulatory role of temperature in effector injection and reinforce the notion that the presence/absence of effectors is not sufficient to predict the outcome of plant-bacteria interactions. Moreover, this work highlights the necessity to study bacterial virulence in a broader set of strains insofar asPtoDC3000 is a reliable model strain but not representative of theP. syringaecomplex.
“…Regarding P. syringae pv. actinidiae , our results confirmed a low-temperature dependency for T3SS efficiency (Puttilli et al ., 2022), which is entirely in line with the environmental conditions – in late winter or early spring – under which P. syringae pv. actinidiae is reported to cause disease or damage in the kiwifruit orchards (Kim et al ., 2017; Donati et al ., 2020).…”
Section: Discussionsupporting
confidence: 91%
“…glycinea could be involved in the regulation of T3SS-related gene expression in response to temperature (Ullrich et al ., 1995). Alternatively, if evidence hints that gene expression is not directly modified by temperature (Puttilli et al ., 2022), thermoregulation might act later in the transcription/translation chain, during T3SS assembly, or on translocation efficiency. In addition, the study of potential differences in membrane fluidity between strains is promising.…”
Section: Discussionmentioning
confidence: 99%
“…For each technical replicate, the conductivity value from the first measure was subtracted to values measured at each successive time points for normalization (Puttilli et al ., 2022). For each strain-temperature modality within each replicated experiment, conductivity was calculated as the average of the values of the three technical replicates for each time point, and ion-leakage curves over time were established accordingly.…”
Section: Methodsmentioning
confidence: 99%
“…On the other hand, for P. syringae pv. actinidiae strains, it was shown that there was no difference in hrpA1 promoter activity in vitro across a temperature range of 18-28°C, nonetheless, substantial differences were evident at a functional level, demonstrating a low-temperature dependency for T3SS efficiency for these strains (Puttilli et al ., 2022). However, the complete implications of warm temperatures on P. syringae virulence in plants remain poorly understood (Li et al ., 2006; Hockett et al ., 2013).…”
ThePseudomonas syringaespecies complex is a very important plant pathogenic bacterium, causing damage and economic losses on many crops. Research efforts for the understanding of the determinants of the host-range of a given strain are considerable. Recently, we showed that the inability of aP. syringaepv.actinidiaestrain to trigger ETI inA. thalianais due to an inefficient T3SS and not to the absence of a recognized effector. In this context, we compared severalP. syringaestrains belonging to different phylogroups and carrying the same plasmid-born avirulence gene for their ability to induce an HR inA. thalianaCol-0, as a marker of T3SS efficiency.PtoDC3000AvrBandPmaM6AvrBconsistently triggered a strong HR while other strains induced it at different intensities significantly depending on temperature. Both behaviors of low and warm temperature-dependency for T3SS efficiency were observed among thermosensitive strains, irrespective of theirin-vitrogrowth optimum. Surprisingly, differences were also observed among quasi-clonal strains. These results reveal a strongly strain-specific regulatory role of temperature in effector injection and reinforce the notion that the presence/absence of effectors is not sufficient to predict the outcome of plant-bacteria interactions. Moreover, this work highlights the necessity to study bacterial virulence in a broader set of strains insofar asPtoDC3000 is a reliable model strain but not representative of theP. syringaecomplex.
“…Interestingly, our results showed that 6 out of 10 isolates exhibited signi cant upregulation of T3SS expression in the presence of sugar beet extract, highlighting the speci city of this system to the sugar beet host and suggesting a specialised mechanism for the delivery of T3Es to this particular plant species. This observation is consistent with the existing literature on pathogens in which host-speci c signalling triggers T3SS expression (Puttilli et al, 2022). Contrary to expectations, the addition of sugar beet extract led to a down-regulation of T3SS expression in certain isolates, including the aforementioned P. corrugata MRh80.…”
The intricate interplay between plants and microorganisms in agricultural ecosystems holds immense potential for increasing crop productivity and resilience in the face of climate change and increasing pathogen pressure. This study addresses the function of the type 3 secretion system (T3SS) in nonpathogenic Pseudomonas strains associated with sugar beet (Beta vulgaris L.). We identified T3SS-positive isolates and characterised their genetic diversity and T3SS expression profiles. Our results show that T3SS is widely distributed among sugar beet-associated Pseudomonas, with variations in T3SS gene sequences and expression patterns. Notably, T3SS functionality was demonstrated in one isolate, P. marginalis OL141. In planta experiments with this isolate showed a correlation between T3SS and the growth of sugar beet and resistance to Pseudomonas syringae infections. The T3SS-mediated interactions in P. marginalis OL141 point to a novel mechanism underlying plant-microbe symbiosis and offer promising opportunities for sustainable agriculture. Future research directions include elucidating the mechanistic basis of T3SS-mediated plant-microbe interactions and exploring their broader implications for sustainable agriculture and global food security.
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