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Fusarium oxysporum triggers tissue-specific transcriptional reprogramming in Arabidopsis thaliana.

Lyons R, Stiller J, Powell J, Rusu A, Manners JM, Kazan K - PLoS ONE (2015)

Bottom Line: At least half of the genes induced or repressed by F. oxysporum showed tissue-specific regulation.Regulators of auxin and ABA signalling, mannose binding lectins and peroxidases showed strong differential expression in root tissue.We demonstrate that ARF2 and PRX33, two genes regulated in the roots, promote susceptibility to F. oxysporum.

View Article: PubMed Central - PubMed

Affiliation: CSIRO Agriculture Flagship, Queensland Bioscience Precinct, Brisbane, QLD, Australia.

ABSTRACT
Some of the most devastating agricultural diseases are caused by root-infecting pathogens, yet the majority of studies on these interactions to date have focused on the host responses of aerial tissues rather than those belowground. Fusarium oxysporum is a root-infecting pathogen that causes wilt disease on several plant species including Arabidopsis thaliana. To investigate and compare transcriptional changes triggered by F. oxysporum in different Arabidopsis tissues, we infected soil-grown plants with F. oxysporum and subjected root and leaf tissue harvested at early and late timepoints to RNA-seq analyses. At least half of the genes induced or repressed by F. oxysporum showed tissue-specific regulation. Regulators of auxin and ABA signalling, mannose binding lectins and peroxidases showed strong differential expression in root tissue. We demonstrate that ARF2 and PRX33, two genes regulated in the roots, promote susceptibility to F. oxysporum. In the leaves, defensins and genes associated with the response to auxin, cold and senescence were strongly regulated while jasmonate biosynthesis and signalling genes were induced throughout the plant.

No MeSH data available.


Related in: MedlinePlus

PRX33 is induced by F. oxysporum and promotes susceptibility to F. oxysporum.(A) The fold induction or repression of peroxidases in response to F. oxysporum. (B) Representative F. oxysporum- inoculated WT and prx33 mutant plants at 14 days post inoculation. (C) Mean disease score and standard error from 16 plants. Asterisk indicates significant difference relative to WT (P<0.01).
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pone.0121902.g004: PRX33 is induced by F. oxysporum and promotes susceptibility to F. oxysporum.(A) The fold induction or repression of peroxidases in response to F. oxysporum. (B) Representative F. oxysporum- inoculated WT and prx33 mutant plants at 14 days post inoculation. (C) Mean disease score and standard error from 16 plants. Asterisk indicates significant difference relative to WT (P<0.01).

Mentions: Numerous peroxidases were strongly induced by F. oxysporum in the roots (Fig 4A). PRX53 is JA-responsive and promotes resistance to the cyst nematode H. schachtii [49] while PRX33 is required for ROS formation in response to F. oxysporum filtrate and is a major contributor of MAMP-triggered ROS production [50, 51]. We inoculated prx33-1 and prx33-2, which contain T-DNA insertions in the first intron of PRX33 with F. oxysporum and found that they were more resistant to F. oxysporum than WT plants suggesting that PRX33 promotes susceptibility to F. oxysporum (Fig 4B and 4C). Interestingly, A. thaliana antisense or T-DNA insertion lines with reduced levels of PRX33 and PRX34 are more susceptible to various bacterial and fungal pathogens [50, 52] and show defective SA signaling and impaired PTI responses [53]. Numerous studies associate ROS production with defence, however recent data suggest that ROS may also promote disease development of necrotrophic pathogens. For example, Medicago truncatula plants with reduced ROS-producing capabilities in the roots show enhanced resistance to the root rot pathogen Aphanomyceseuteiches [54]; transgenic potato plants that produce increased levels of pathogen-inducible ROS are more susceptible to Alternaria solani [55] while RBOHB-generated ROS promotes Botrytis cinerea lesion development in Nicotiana benthamiana [56]. In addition to basal defence signaling and modulation of defence responses such as the hypersensitive response and cell wall cross linking, ROS affect diverse physiological processes including regulation of lateral root emergence [57] and leaf senescence [58]. Indeed, prx33/prx34 knockdown plants show delayed senescence [59]. A possible explanation for PRX33-mediated susceptibility to F. oxysporum is that that PRX33- generated ROS in the roots acts as a systemic signal to accelerate senescence in the leaves, promoting the transition from a biotrophic to necrotrophic lifestyle of F. oxysporum.


Fusarium oxysporum triggers tissue-specific transcriptional reprogramming in Arabidopsis thaliana.

Lyons R, Stiller J, Powell J, Rusu A, Manners JM, Kazan K - PLoS ONE (2015)

PRX33 is induced by F. oxysporum and promotes susceptibility to F. oxysporum.(A) The fold induction or repression of peroxidases in response to F. oxysporum. (B) Representative F. oxysporum- inoculated WT and prx33 mutant plants at 14 days post inoculation. (C) Mean disease score and standard error from 16 plants. Asterisk indicates significant difference relative to WT (P<0.01).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4388846&req=5

pone.0121902.g004: PRX33 is induced by F. oxysporum and promotes susceptibility to F. oxysporum.(A) The fold induction or repression of peroxidases in response to F. oxysporum. (B) Representative F. oxysporum- inoculated WT and prx33 mutant plants at 14 days post inoculation. (C) Mean disease score and standard error from 16 plants. Asterisk indicates significant difference relative to WT (P<0.01).
Mentions: Numerous peroxidases were strongly induced by F. oxysporum in the roots (Fig 4A). PRX53 is JA-responsive and promotes resistance to the cyst nematode H. schachtii [49] while PRX33 is required for ROS formation in response to F. oxysporum filtrate and is a major contributor of MAMP-triggered ROS production [50, 51]. We inoculated prx33-1 and prx33-2, which contain T-DNA insertions in the first intron of PRX33 with F. oxysporum and found that they were more resistant to F. oxysporum than WT plants suggesting that PRX33 promotes susceptibility to F. oxysporum (Fig 4B and 4C). Interestingly, A. thaliana antisense or T-DNA insertion lines with reduced levels of PRX33 and PRX34 are more susceptible to various bacterial and fungal pathogens [50, 52] and show defective SA signaling and impaired PTI responses [53]. Numerous studies associate ROS production with defence, however recent data suggest that ROS may also promote disease development of necrotrophic pathogens. For example, Medicago truncatula plants with reduced ROS-producing capabilities in the roots show enhanced resistance to the root rot pathogen Aphanomyceseuteiches [54]; transgenic potato plants that produce increased levels of pathogen-inducible ROS are more susceptible to Alternaria solani [55] while RBOHB-generated ROS promotes Botrytis cinerea lesion development in Nicotiana benthamiana [56]. In addition to basal defence signaling and modulation of defence responses such as the hypersensitive response and cell wall cross linking, ROS affect diverse physiological processes including regulation of lateral root emergence [57] and leaf senescence [58]. Indeed, prx33/prx34 knockdown plants show delayed senescence [59]. A possible explanation for PRX33-mediated susceptibility to F. oxysporum is that that PRX33- generated ROS in the roots acts as a systemic signal to accelerate senescence in the leaves, promoting the transition from a biotrophic to necrotrophic lifestyle of F. oxysporum.

Bottom Line: At least half of the genes induced or repressed by F. oxysporum showed tissue-specific regulation.Regulators of auxin and ABA signalling, mannose binding lectins and peroxidases showed strong differential expression in root tissue.We demonstrate that ARF2 and PRX33, two genes regulated in the roots, promote susceptibility to F. oxysporum.

View Article: PubMed Central - PubMed

Affiliation: CSIRO Agriculture Flagship, Queensland Bioscience Precinct, Brisbane, QLD, Australia.

ABSTRACT
Some of the most devastating agricultural diseases are caused by root-infecting pathogens, yet the majority of studies on these interactions to date have focused on the host responses of aerial tissues rather than those belowground. Fusarium oxysporum is a root-infecting pathogen that causes wilt disease on several plant species including Arabidopsis thaliana. To investigate and compare transcriptional changes triggered by F. oxysporum in different Arabidopsis tissues, we infected soil-grown plants with F. oxysporum and subjected root and leaf tissue harvested at early and late timepoints to RNA-seq analyses. At least half of the genes induced or repressed by F. oxysporum showed tissue-specific regulation. Regulators of auxin and ABA signalling, mannose binding lectins and peroxidases showed strong differential expression in root tissue. We demonstrate that ARF2 and PRX33, two genes regulated in the roots, promote susceptibility to F. oxysporum. In the leaves, defensins and genes associated with the response to auxin, cold and senescence were strongly regulated while jasmonate biosynthesis and signalling genes were induced throughout the plant.

No MeSH data available.


Related in: MedlinePlus