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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

Auxin-related phenotypes and role of ARF2 in the A. thaliana—F. oxysporum interaction.(A) F. oxysporum inoculation triggers root growth inhibition and lateral root (LR) proliferation in agar-grown Col-0 seedlings. (i) Two week old seedlings were inoculated with water (mock) or F. oxysporum and photographed at 9 days post inoculation. (ii) Mean primary root (PR) length or (iii) mean number of LRs per cm PR in mock or F. oxysporum—inoculated agar-grown seedlings measured at 9 dpi. (B) F. oxysporum inoculation triggers root growth inhibition in soil-grown Col-0 plants. Mean PR length in mock (grey bars) or F. oxysporum (black bars)–inoculated soil-grown plants at 1, 6 and 14 dpi. Data shown are mean and standard error from >13 plants. Asterisk indicates significant difference between mock and F. oxysporum treatment (P<0.05). (C) Representative F. oxysporum- inoculated WT (Col-0) and mutant plants at 14 days post inoculation (dpi). (D) Mean percentage of diseased leaves per plant and standard error from at least 30 plants per line. Asterisks indicate significant difference relative to WT (*P<0.05; **P<0.01).
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pone.0121902.g005: Auxin-related phenotypes and role of ARF2 in the A. thaliana—F. oxysporum interaction.(A) F. oxysporum inoculation triggers root growth inhibition and lateral root (LR) proliferation in agar-grown Col-0 seedlings. (i) Two week old seedlings were inoculated with water (mock) or F. oxysporum and photographed at 9 days post inoculation. (ii) Mean primary root (PR) length or (iii) mean number of LRs per cm PR in mock or F. oxysporum—inoculated agar-grown seedlings measured at 9 dpi. (B) F. oxysporum inoculation triggers root growth inhibition in soil-grown Col-0 plants. Mean PR length in mock (grey bars) or F. oxysporum (black bars)–inoculated soil-grown plants at 1, 6 and 14 dpi. Data shown are mean and standard error from >13 plants. Asterisk indicates significant difference between mock and F. oxysporum treatment (P<0.05). (C) Representative F. oxysporum- inoculated WT (Col-0) and mutant plants at 14 days post inoculation (dpi). (D) Mean percentage of diseased leaves per plant and standard error from at least 30 plants per line. Asterisks indicate significant difference relative to WT (*P<0.05; **P<0.01).

Mentions: Exogenous treatment with auxin does not alter the response of A. thaliana plants to F. oxysporum, however several mutants compromised in auxin signalling and transport show increased resistance to F. oxysporum, suggesting that auxin promotes susceptibility to F. oxysporum [11, 75]. In agar-grown seedlings, a marked inhibition of root elongation and increased lateral root proliferation is evident in F. oxysporum–inoculated seedlings relative to mock inoculated seedlings (Fig 5A). Similarly, roots of soil-grown F. oxysporum-inoculated plants are shorter and appear bushier relative to mock-inoculated plants by 6 dpi (Fig 1A, Fig 5B). Such phenotypes are reminiscent of plants treated with auxin. Given that F. oxysporum enters the plant through lateral root (LR) initials [11, 76], an increased proliferation of LR might aid F. oxysporum infection. Several genes differentially expressed >2 fold in the roots, including CONSTANS-LIKE 3 (COL3), ARF19, IAA14 [77], IAA28 [78] and the chitinase-like protein CTL1 [79] regulate lateral root growth or formation. CALLOSE SYNTHASE 3 (CS3; AT5G13000) inhibits callose accumulation in emerging lateral roots [80]. Strong repression of (>8 fold) of CS3 in the roots at 6 dpi may be a mechanism to increase physical barriers against F. oxysporum entry.


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)

Auxin-related phenotypes and role of ARF2 in the A. thaliana—F. oxysporum interaction.(A) F. oxysporum inoculation triggers root growth inhibition and lateral root (LR) proliferation in agar-grown Col-0 seedlings. (i) Two week old seedlings were inoculated with water (mock) or F. oxysporum and photographed at 9 days post inoculation. (ii) Mean primary root (PR) length or (iii) mean number of LRs per cm PR in mock or F. oxysporum—inoculated agar-grown seedlings measured at 9 dpi. (B) F. oxysporum inoculation triggers root growth inhibition in soil-grown Col-0 plants. Mean PR length in mock (grey bars) or F. oxysporum (black bars)–inoculated soil-grown plants at 1, 6 and 14 dpi. Data shown are mean and standard error from >13 plants. Asterisk indicates significant difference between mock and F. oxysporum treatment (P<0.05). (C) Representative F. oxysporum- inoculated WT (Col-0) and mutant plants at 14 days post inoculation (dpi). (D) Mean percentage of diseased leaves per plant and standard error from at least 30 plants per line. Asterisks indicate significant difference relative to WT (*P<0.05; **P<0.01).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4388846&req=5

pone.0121902.g005: Auxin-related phenotypes and role of ARF2 in the A. thaliana—F. oxysporum interaction.(A) F. oxysporum inoculation triggers root growth inhibition and lateral root (LR) proliferation in agar-grown Col-0 seedlings. (i) Two week old seedlings were inoculated with water (mock) or F. oxysporum and photographed at 9 days post inoculation. (ii) Mean primary root (PR) length or (iii) mean number of LRs per cm PR in mock or F. oxysporum—inoculated agar-grown seedlings measured at 9 dpi. (B) F. oxysporum inoculation triggers root growth inhibition in soil-grown Col-0 plants. Mean PR length in mock (grey bars) or F. oxysporum (black bars)–inoculated soil-grown plants at 1, 6 and 14 dpi. Data shown are mean and standard error from >13 plants. Asterisk indicates significant difference between mock and F. oxysporum treatment (P<0.05). (C) Representative F. oxysporum- inoculated WT (Col-0) and mutant plants at 14 days post inoculation (dpi). (D) Mean percentage of diseased leaves per plant and standard error from at least 30 plants per line. Asterisks indicate significant difference relative to WT (*P<0.05; **P<0.01).
Mentions: Exogenous treatment with auxin does not alter the response of A. thaliana plants to F. oxysporum, however several mutants compromised in auxin signalling and transport show increased resistance to F. oxysporum, suggesting that auxin promotes susceptibility to F. oxysporum [11, 75]. In agar-grown seedlings, a marked inhibition of root elongation and increased lateral root proliferation is evident in F. oxysporum–inoculated seedlings relative to mock inoculated seedlings (Fig 5A). Similarly, roots of soil-grown F. oxysporum-inoculated plants are shorter and appear bushier relative to mock-inoculated plants by 6 dpi (Fig 1A, Fig 5B). Such phenotypes are reminiscent of plants treated with auxin. Given that F. oxysporum enters the plant through lateral root (LR) initials [11, 76], an increased proliferation of LR might aid F. oxysporum infection. Several genes differentially expressed >2 fold in the roots, including CONSTANS-LIKE 3 (COL3), ARF19, IAA14 [77], IAA28 [78] and the chitinase-like protein CTL1 [79] regulate lateral root growth or formation. CALLOSE SYNTHASE 3 (CS3; AT5G13000) inhibits callose accumulation in emerging lateral roots [80]. Strong repression of (>8 fold) of CS3 in the roots at 6 dpi may be a mechanism to increase physical barriers against F. oxysporum entry.

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