The immunity of Meiwa kumquat against Xanthomonas citri is associated with a known susceptibility gene induced by a transcription activator-like effector

Teper, Doron; Xu, Jin; Li, Jinyun; Wang, Nian

doi:10.1371/journal.ppat.1008886

Cited by 26 publications

(25 citation statements)

References 86 publications

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“…It has been reported that cultivated citrus varieties are more susceptible to canker disease than wild citrus, and that wild citrus varieties have a broad spectrum of disease resistance, whereas cultivated citrus varieties have lost certain resistance to different degrees during domestication [2,6]. For example, Meiwa kumquat obtain a durable resistance to Xcc by upregulating a host susceptibility gene to elicit immune responses [31]. Tracing back to wild germplams is an alternative strategy for identifying gene resources for breeding purpose.…”

Section: Discussionmentioning

confidence: 99%

Natural variations of TFIIAγ gene and LOB1 promoter contribute to citrus canker disease resistance in Atalantia buxifolia

et al. 2021

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Citrus canker caused by Xanthomonas citri subsp. citri (Xcc) is one of the most devastating diseases in citrus industry worldwide. Most citrus cultivars such as sweet orange are susceptible to canker disease. Here, we utilized wild citrus to identify canker-resistant germplasms, and found that Atalantia buxifolia, a primitive (distant-wild) citrus, exhibited remarkable resistance to canker disease. Although the susceptibility gene LATERAL ORGAN BOUNDARIES 1 (LOB1) could also be induced in Atalantia after canker infection, the induction extent was far lower than that in sweet orange. In addition, three of amino acids encoded by transcription factor TFIIAγ in Atalantia (AbTFIIAγ) exhibited difference from those in sweet orange (CsTFIIAγ) which could stabilize the interaction between effector PthA4 and effector binding element (EBE) of LOB1 promoter. The mutation of AbTFIIAγ did not change its interaction with transcription factor binding motifs (TFBs). However, the AbTFIIAγ could hardly support the LOB1 expression induced by the PthA4. In addition, the activity of AbLOB1 promoter was significantly lower than that of CsLOB1 under the induction by PthA4. Our results demonstrate that natural variations of AbTFIIAγ and effector binding element (EBE) in the AbLOB1 promoter are crucial for the canker disease resistance of Atalantia. The natural mutations of AbTFIIAγ gene and AbLOB1 promoter in Atalantia provide candidate targets for improving the resistance to citrus canker disease.

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Section: Discussionmentioning

confidence: 99%

Natural variations of TFIIAγ gene and LOB1 promoter contribute to citrus canker disease resistance in Atalantia buxifolia

et al. 2021

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“…Designer TALEs (dTALEs) containing the repeat arrays elaborated in Fig 3A were constructed using “Golden Gate TALEN and TAL Effector Kit 2.0” as previously described [ 77 ] and cloned into pTAL2 as a final destination vector. The pTAL2 PstI/EcoRI fragments containing the dTALEs were cloned into pBBRNPth [ 54 ] and transformed into Xcc pthA4 :Tn5 [ 61 ] by electroporation. Expression of all constructed dTALEs and their adapted derivatives in Xcc was validated by Western blot [ 78 ] using Anti-HA High Affinity antibody (Roche diagnostics, Basel, Switzerland) ( S4 Fig ).…”

Section: Methodsmentioning

confidence: 99%

“…Ralstonia solanacearum strains that experimentally evolved on bean plants harbored a mutation in the transcriptional regulator efpR , which regulates EPS production, motility and numerous metabolic processes [ 51 , 52 ]. Xcc strains that evolved in resistant Meiwa kumquat via repeated inoculation and isolation harbored point mutations in the pthA4 TALE that was later verified to be associated with elicitation of immune responses [ 53 , 54 ].…”

Section: Introductionmentioning

confidence: 99%

Consequences of adaptation of TAL effectors on host susceptibility to Xanthomonas

Teper

Wang

2021

PLoS Genet

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Transcription activator-like effectors (TALEs) are virulence factors of Xanthomonas that induce the expression of host susceptibility (S) genes by specifically binding to effector binding elements (EBEs) in their promoter regions. The DNA binding specificity of TALEs is dictated by their tandem repeat regions, which are highly variable between different TALEs. Mutation of the EBEs of S genes is being utilized as a key strategy to generate resistant crops against TALE-dependent pathogens. However, TALE adaptations through rearrangement of their repeat regions is a potential obstacle for successful implementation of this strategy. We investigated the consequences of TALE adaptations in the citrus pathogen Xanthomonas citri subsp. citri (Xcc), in which PthA4 is the TALE required for pathogenicity, whereas CsLOB1 is the corresponding susceptibility gene, on host resistance. Seven TALEs, containing two-to-nine mismatching-repeats to the EBEPthA4 that were unable to induce CsLOB1 expression, were introduced into Xcc pthA4:Tn5 and adaptation was simulated by repeated inoculations into and isolations from sweet orange for a duration of 30 cycles. While initially all strains failed to promote disease, symptoms started to appear between 9–28 passages in four TALEs, which originally harbored two-to-five mismatches. Sequence analysis of adapted TALEs identified deletions and mutations within the TALE repeat regions which enhanced putative affinity to the CsLOB1 promoter. Sequence analyses suggest that TALEs adaptations result from recombinations between repeats of the TALEs. Reintroduction of these adapted TALEs into Xcc pthA4:Tn5 restored the ability to induce the expression of CsLOB1, promote disease symptoms and colonize host plants. TALEs harboring seven-to-nine mismatches were unable to adapt to overcome the incompatible interaction. Our study experimentally documented TALE adaptations to incompatible EBE and provided strategic guidance for generation of disease resistant crops against TALE-dependent pathogens.

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“…Intriguingly, Xanthomonas citri subsp. citri, another bacterial pathogen of citrus, infection of kumquat ( Citrus japonica , syn: Fortunella crassifolia ) triggers H2O2 production at 2 days after inoculation which peaks (9.86 µmol g −1 FW) at 8 days after inoculation, eventually leading to cell death 23, 24 . X. citri subsp.…”

Section: Hlb Caused Cell Death Is Instigated By Rosmentioning

confidence: 99%

“…X. citri subsp. citri induced cell death is a slow process and happens at approximately 6-8 days after inoculation 24 . Hence, we conjectured that ROS induced by CLas reaches the threshold necessary to trigger the death of companion and sieve element cells in mature leaves, but possibly not in the early stage of infection of young leaves before CLas titers reach a certain threshold.…”

Section: Hlb Caused Cell Death Is Instigated By Rosmentioning

confidence: 99%

Citrus Huanglongbing is an immune-mediated disease that can be treated by mitigating reactive oxygen species triggered cell death of the phloem tissues caused by Candidatus Liberibacter asiaticus

Pang

Huang

et al. 2021

Preprint

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The immune system is critical for keeping animals and plants healthy from pathogens. However, immune-mediated diseases are also common for human. Immune-mediated diseases have not been reported for plants. Here, we present evidence that citrus Huanglongbing (HLB), caused by phloem-colonizing Candidatus Liberibacter asiaticus (CLas), is an immune-mediated disease. CLas infection of Citrus sinensis stimulated systemic and chronic immune response in the phloem tissues including reactive oxygen species (ROS) production as indicated by H2O2, callose deposition, and induction of immune related genes. Systemic cell death of companion and sieve element cells, but not surrounding parenchyma cells, was observed following ROS production triggered by CLas. ROS production triggered by CLas localized in phloem tissues. The H2O2 concentration in exudates extracted from phloem enriched bark tissue of CLas infected plants reached a threshold of killing citrus protoplast cells, which was suppressed by uric acid (a ROS scavenger) and gibberellin. Foliar spray of HLB positive citrus with antioxidants (uric acid and rutin) and gibberellin significantly reduced both H2O2 concentrations and cell death in phloem tissues induced by CLas and reduced HLB symptoms. RNA-seq analyses of CLas infected and health C. sinensis support that CLas causes oxidative stress. In sum, HLB is an immune-mediated disease and both mitigating ROS via antioxidants and promoting plant growth can reduce cell death of the phloem tissues caused by CLas, thus controlling HLB.

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The immunity of Meiwa kumquat against Xanthomonas citri is associated with a known susceptibility gene induced by a transcription activator-like effector

Cited by 26 publications

References 86 publications

Natural variations of TFIIAγ gene and LOB1 promoter contribute to citrus canker disease resistance in Atalantia buxifolia

Natural variations of TFIIAγ gene and LOB1 promoter contribute to citrus canker disease resistance in Atalantia buxifolia

Consequences of adaptation of TAL effectors on host susceptibility to Xanthomonas

Citrus Huanglongbing is an immune-mediated disease that can be treated by mitigating reactive oxygen species triggered cell death of the phloem tissues caused by Candidatus Liberibacter asiaticus

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