Impairment of Cellulose Synthases Required for<i>Arabidopsis</i>Secondary Cell Wall Formation Enhances Disease Resistance

Hernández-Blanco, Camilo; Feng, Dong Xin; Hu, Jian; Sánchez‐Vallet, Andrea; Deslandes, Laurent; Llorente, Francisco Rubio; Berrocal-Lobo, Marta; Keller, Harald; Barlet, Xavier; Sánchez‐Rodríguez, Clara; Anderson, Lisa K.; Somerville, Shauna; Marco, Yves; Molina, Antonio

doi:10.1105/tpc.106.048058

Cited by 410 publications

(459 citation statements)

References 87 publications

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“…The fact that coi1 has enhanced susceptibility to most foliar necrotrophic fungi (Thomma et al, 1998;Lorenzo et al, 2004;Guo and Stotz, 2007;Hernandez-Blanco et al, 2007), but increased resistance to F. oxysporum, suggests that other root-infecting fungi might actively use the JA signaling pathway to promote disease. However, coi1 also displays enhanced susceptibility to the soil-borne oomycete pathogens Pythium irregulare (Adie et al, 2007) and Pythium mastophorum (Vijayan et al, 1998), as well as the vascular wilt-inciting fungal pathogen Verticillium longispo- rum (Johansson et al, 2006), suggesting that the effect of the coi1 mutation in restricting disease symptom development is more specific to F. oxysporum.…”

Section: Discussionmentioning

confidence: 99%

Fusarium oxysporum hijacks COI1‐mediated jasmonate signaling to promote disease development in Arabidopsis

Thatcher

Manners

Kazan³

2009

The Plant Journal

269

298

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SUMMARYAlthough defense responses mediated by the plant oxylipin jasmonic acid (JA) are often necessary for resistance against pathogens with necrotrophic lifestyles, in this report we demonstrate that jasmonate signaling mediated through COI1 in Arabidopsis thaliana is responsible for susceptibility to wilt disease caused by the root-infecting fungal pathogen Fusarium oxysporum. Despite compromised JA-dependent defense responses, the JA perception mutant coronatine insensitive 1 (coi1), but not JA biosynthesis mutants, exhibited a high level of resistance to wilt disease caused by F. oxysporum. This response was independent from salicylic acid-dependent defenses, as coi1/NahG plants showed similar disease resistance to coi1 plants. Inoculation of reciprocal grafts made between coi1 and wild-type plants revealed that coi1-mediated resistance occurred primarily through the coi1 rootstock tissues. Furthermore, microscopy and quantification of fungal DNA during infection indicated that coi1-mediated resistance was not associated with reduced fungal penetration and colonization until a late stage of infection, when leaf necrosis was highly developed in wild-type plants. In contrast to wild-type leaves, coi1 leaves showed no necrosis following the application of F. oxysporum culture filtrate, and showed reduced expression of senescence-associated genes during disease development, suggesting that coi1 resistance is most likely achieved through the inhibition of F. oxysporum-incited lesion development and plant senescence. Together, our results indicate that F. oxysporum hijacks non-defensive aspects of the JA-signaling pathway to cause wilt-disease symptoms that lead to plant death in Arabidopsis.

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Section: Discussionmentioning

confidence: 99%

Fusarium oxysporum hijacks COI1‐mediated jasmonate signaling to promote disease development in Arabidopsis

Thatcher

Manners

Kazan³

2009

The Plant Journal

269

298

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“…Thus, the ABA biosynthesis pathway is also required for the full virulence of the obligate oomycete pathogen H. arabidopsis in terms of asexual spore production and proliferating hyphal growth, while ABA positively regulates resistance against necrotrophic A. brassicicola infection, indicating strikingly different roles of ABA in the interactions with bio/hemibiotrophs and necrotrophs. However, contradictory roles of ABA in other pathosystems have also been documented; for example, ABA suppresses resistance to necrotrophic pathogens, including Botrytis cinerea, Fusarium oxysporum, Plectosphaerella cucumerina, and Erwinia chrysanthemi (Audenaert et al, 2002;Anderson et al, 2004;Hernandez-Blanco et al, 2007;Asselbergh et al, 2008b), and ABA signaling may positively regulate the RLM1 Col determined resistance to the hemibiotrophic fungal pathogen Leptosphaeria maculans and the edr1-mediated resistance to the obligate biotrophic powdery mildew pathogen Golovinomyces cichoracearum in Arabidopsis (Kaliff, et al, 2007;Wawrzynska et al, 2008). Hence, specific manifestations of the emerging new role for the abiotic stress signal ABA in modulating disease resistance may depend not only on pathogen lifestyle and overall infection biology but also on specialized features of each interaction, indicating that complex nuanced mechanisms underlie ABA modulation of plant biotic stresses.…”

Section: Discussionmentioning

confidence: 99%

“…This accords with the observation that flg22 peptide induced basal resistance, which is largely independent of SA, JA, or ET signaling pathways in suppressing growth of virulent bacteria (Zipfel et al, 2004;Tsuda et al, 2008), was also suppressed in the cds2-1D mutant. Likewise, the enhanced resistance to the soil-borne bacterium Ralstonia solanacearum in Arabidopsis mutants compromised in secondary cell wall formation is not dependent on SA, JA, or ET but closely associated with ABA biosynthesis and signaling pathways (Hernandez-Blanco et al, 2007). Recent findings that ABA acts as a proinflammatory cytokine in granulocytes (Bruzzone et al, 2007), which requires cADP-Rib as second messenger, is a reminiscent of some aspects of ABA signaling in the plant response to abiotic stresses (Wu et al, 1997;Sanchez et al, 2004).…”

Section: Aba Modulation Of Plant Disease Resistance Mechanismsmentioning

confidence: 99%

Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions

et al. 2009

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We isolated an activation-tagged Arabidopsis (Arabidopsis thaliana) line, constitutive disease susceptibility2-1D (cds2-1D), that showed enhanced bacterial growth when challenged with various Pseudomonas syringae strains. Systemic acquired resistance and systemic PATHOGENESIS-RELATED GENE1 induction were also compromised in cds2-1D. The T-DNA insertion adjacent to NINE-CIS-EPOXYCAROTENOID DIOXYGENASE5 (NCED5), one of six genes encoding the abscisic acid (ABA) biosynthetic enzyme NCED, caused a massive increase in transcript level and enhanced ABA levels .2-fold. Overexpression of NCED genes recreated the enhanced disease susceptibility phenotype. NCED2, NCED3, and NCED5 were induced, and ABA accumulated strongly following compatible P. syringae infection. The ABA biosynthetic mutant aba3-1 showed reduced susceptibility to virulent P. syringae, and ABA, whether through exogenous application or endogenous accumulation in response to mild water stress, resulted in increased bacterial growth following challenge with virulent P. syringae, indicating that ABA suppresses resistance to P. syringae. Likewise ABA accumulation also compromised resistance to the biotrophic oomycete Hyaloperonospora arabidopsis, whereas resistance to the fungus Alternaria brassicicola was enhanced in cds2-1D plants and compromised in aba3-1 plants, indicating that ABA promotes resistance to this necrotroph. Comparison of the accumulation of salicylic acid and jasmonic acid in the wild type, cds2-1D, and aba3-1 plants challenged with P. syringae showed that ABA promotes jasmonic acid accumulation and exhibits a complex antagonistic relationship with salicylic acid. Our findings provide genetic evidence that the abiotic stress signal ABA also has profound roles in modulating diverse plantpathogen interactions mediated at least in part by cross talk with the jasmonic acid and salicylic acid biotic stress signal pathways.

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“…Recent studies demonstrated the importance of the cell wall in immune responses against diverse pathogens [61][62][63][64][65]. Thickness or reinforcement of the cell wall plays important roles in counteracting the penetration of fungal pathogens [66,67].…”

Section: Discussionmentioning

confidence: 99%

Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence

Zhong

et al. 2011

Cell Res

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Emerging evidence suggests that E3 ligases play critical roles in diverse biological processes, including innate immune responses in plants. However, the mechanism of the E3 ligase involvement in plant innate immunity is unclear. We report that a rice gene, OsBBI1, encoding a RING finger protein with E3 ligase activity, mediates broad-spectrum disease resistance. The expression of OsBBI1 was induced by rice blast fungus Magnaporthe oryzae, as well as chemical inducers, benzothiadiazole and salicylic acid. Biochemical analysis revealed that OsBBI1 protein possesses E3 ubiquitin ligase activity in vitro. Genetic analysis revealed that the loss of OsBBI1 function in a Tos17-insertion line increased susceptibility, while the overexpression of OsBBI1 in transgenic plants conferred enhanced resistance to multiple races of M. oryzae. This indicates that OsBBI1 modulates broad-spectrum resistance against the blast fungus. The OsBBI1-overexpressing plants showed higher levels of H 2 O 2 accumulation in cells and higher levels of phenolic compounds and cross-linking of proteins in cell walls at infection sites by M. oryzae compared with wild-type (WT) plants. The cell walls were thicker in the OsBBI1-overexpressing plants and thinner in the mutant plants than in the WT plants. Our results suggest that OsBBI1 modulates broad-spectrum resistance to blast fungus by modifying cell wall defence responses. The functional characterization of OsBBI1 provides insight into the E3 ligase-mediated innate immunity, and a practical tool for constructing broad-spectrum resistance against the most destructive disease in rice.

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Impairment of Cellulose Synthases Required forArabidopsisSecondary Cell Wall Formation Enhances Disease Resistance

Cited by 410 publications

References 87 publications

Fusarium oxysporum hijacks COI1‐mediated jasmonate signaling to promote disease development in Arabidopsis

Fusarium oxysporum hijacks COI1‐mediated jasmonate signaling to promote disease development in Arabidopsis

Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions

Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence

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