The durable wheat disease resistance gene <i>Lr34</i> confers common rust and northern corn leaf blight resistance in maize

Sucher, Justine; Böni, Rainer; Yang, Ping; Rogowsky, Peter; Büchner, Heike; Kastner, Christine; Kumlehn, Jochen; Krattinger, Simon G.; Keller, Beat

doi:10.1111/pbi.12647

Cited by 87 publications

(63 citation statements)

References 71 publications

(105 reference statements)

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“…[5] In contrast to wheat, where Lr34 is only expressed at adult plant stage, barley and rice already showed Lr34 resistance at seedling stage. Therefore, transgenic barley and rice plants offered a valuable tool to study the molecular differences in pathogen resistance caused by Lr34.…”

Section: Introductionmentioning

confidence: 98%

Combined GC- and UHPLC-HR-MS Based Metabolomics to Analyze Durable Anti-fungal Resistance Processes in Cereals

Bucher

Veyel²,

Willmitzer³

et al. 2017

Chimia

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Introduction of durable resistance genes in crops is an important strategy to prevent yield loss caused by pathogens. The durable multi-pathogen resistance gene Lr34 originating from wheat is widely used in breeding, and is functionally transferable to barley and rice. The molecular resistance mechanism of Lr34, encoding for an adenosine triphosphate-binding cassette transporter, is not known yet. To understand the molecular function and the defense response of durable disease resistance in cereals, the metabolic response of Lr34 was investigated in, except for the Lr34 gene, genetically identical lines of barley, rice and wheat. A broad range of compounds including primary, secondary and lipophilic metabolites were analyzed by a combination of gas (GC) and liquid chromatography (LC) mass spectrometry (MS) based methods. Data from metabolomics correlated well with transcriptomics data for plant defense responses such as the formation of anti-fungal hordatines or the components of the glyoxylate cycle. Induction of the glyoxylate cycle found in transgenic Lr34 rice grown in the greenhouse was confirmed in field-grown natural Lr34 wheat. Constitutively active plant defense responses were observed in the different cereals. SCS-Metrohm Award for best oral presentation in Analytical SciencesAbstract: Introduction of durable resistance genes in crops is an important strategy to prevent yield loss caused by pathogens. The durable multi-pathogen resistance gene Lr34 originating from wheat is widely used in breeding, and is functionally transferable to barley and rice. The molecular resistance mechanism of Lr34, encoding for an adenosine triphosphate-binding cassette transporter, is not known yet. To understand the molecular function and the defense response of durable disease resistance in cereals, the metabolic response of Lr34 was investigated in, except for the Lr34 gene, genetically identical lines of barley, rice and wheat. A broad range of compounds including primary, secondary and lipophilic metabolites were analyzed by a combination of gas (GC) and liquid chromatography (LC) mass spectrometry (MS) based methods. Data from metabolomics correlated well with transcriptomics data for plant defense responses such as the formation of anti-fungal hordatines or the components of the glyoxylate cycle. Induction of the glyoxylate cycle found in transgenic Lr34 rice grown in the greenhouse was confirmed in field-grown natural Lr34 wheat. Constitutively active plant defense responses were observed in the different cereals.

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Section: Introductionmentioning

confidence: 98%

Combined GC- and UHPLC-HR-MS Based Metabolomics to Analyze Durable Anti-fungal Resistance Processes in Cereals

Bucher

Veyel²,

Willmitzer³

et al. 2017

Chimia

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“…All resistant wheat cultivars carry the same Lr34 allele ( Lr34res ) that evolved from an ancestral, susceptible allele ( Lr34sus ) after wheat domestication by two gain‐of‐function mutations (Krattinger et al ., ). Lr34res is functionally transferrable into all major cereals as a transgene, including barley ( Hordeum vulgare ), rice ( Oryza sativa ), maize ( Zea mays ), and sorghum ( Sorghum bicolor ) (Risk et al ., ; Krattinger et al ., ; Sucher et al ., ; Schnippenkoetter et al ., ; Boni et al ., ). In these cereal species, Lr34res resulted in enhanced resistance against various biotrophic or hemi‐biotrophic fungal pathogens, as well as in the development of LTN.…”

Section: Introductionmentioning

confidence: 99%

Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene Lr34

et al. 2019

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Summary The wheat Lr34res allele, coding for an ATP ‐binding cassette transporter, confers durable resistance against multiple fungal pathogens. The Lr34sus allele, differing from Lr34res by two critical nucleotide polymorphisms, is found in susceptible wheat cultivars. Lr34res is functionally transferrable as a transgene into all major cereals, including rice, barley, maize, and sorghum. Here, we used transcriptomics, physiology, genetics, and in vitro and in vivo transport assays to study the molecular function of Lr34 . We report that Lr34res results in a constitutive induction of transcripts reminiscent of an abscisic acid ( ABA )‐regulated response in transgenic rice. Lr34‐ expressing rice was altered in biological processes that are controlled by this phytohormone, including dehydration tolerance, transpiration and seedling growth. In planta seedling and in vitro yeast accumulation assays revealed that both LR 34res and LR 34sus act as ABA transporters. However, whereas the LR 34res protein was detected in planta the LR 34sus version was not, suggesting a post‐transcriptional regulatory mechanism. Our results identify ABA as a substrate of the LR 34 ABC transporter. We conclude that LR 34res‐mediated ABA redistribution has a major effect on the transcriptional response and physiology of Lr34res ‐expressing plants and that ABA is a candidate molecule that contributes to Lr34res ‐mediated disease resistance.

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“…In the present study, disease development was slower and pathogen growth reduced on Lr34 ‐transgenic plants, as already described by using chitin quantification (Boni et al ., ). This has also been reported for various other fungal pathogens such as M. oryzae and Puccinia sorghi in transgenic Lr34 rice (Krattinger et al ., ) and maize (Sucher et al ., ).…”

Section: Discussionmentioning

confidence: 97%

“…Sucher et al . () have also suggested that the resistance could occur during the prehaustorium or feeding structure formation stage; this is the infection step common to both biotrophic and hemibiotrophic pathogens affected by Lr34 . Rubiales & Niks () showed that the reduction of infection frequency and the increase of latency period provided by Lr34 was associated with a reduction of haustorium formation and a lower rate of intercellular hyphal development.…”

Section: Discussionmentioning

confidence: 99%

Transcriptional profiling reveals no response of fungal pathogens to the durable, quantitative Lr34 disease resistance gene of wheat

et al. 2017

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Durable resistance against fungal pathogens is highly valuable for disease management in agriculture. For its sustainable use, and to avoid pathogen adaptation, it is important to understand the underlying molecular mechanisms. Many studies on durable disease resistance in plants have focused exclusively on the host plant, whereas possible reactions and adaptations of pathogens exposed to this type of resistance have not been well researched. The wheat Lr34 gene, encoding a putative ABC‐transporter, provides broad‐spectrum and durable resistance against multiple fungal pathogens in wheat and is functional as a transgene in all major cereals. Lr34‐based resistance is partial, meaning pathogens can grow and reproduce to some degree on Lr34‐containing plants. Therefore, Lr34‐expressing plants are ideal for studying the response of pathogens to partial resistance. Here, transcriptomic responses of the two fungal pathogens Blumeria graminis f. sp. hordei (barley powdery mildew) and Puccinia triticina (wheat leaf rust) during growth on their respective host plants containing Lr34 were compared to their responses on control plants without Lr34. Two different time points after inoculation were chosen for analysis of powdery mildew on barley and one time point for wheat leaf rust. Transcriptome analyses revealed that there were no differences in the expression patterns of the two pathogens growing on susceptible versus partially resistant plants, even though pathogen growth was reduced in the presence of Lr34. This reflects the absence of observable reaction in the pathogen to the presence of the Lr34 resistance gene and, consequently, no major alteration of fungal pathogen metabolism.

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The durable wheat disease resistance gene Lr34 confers common rust and northern corn leaf blight resistance in maize

Cited by 87 publications

References 71 publications

Combined GC- and UHPLC-HR-MS Based Metabolomics to Analyze Durable Anti-fungal Resistance Processes in Cereals

Combined GC- and UHPLC-HR-MS Based Metabolomics to Analyze Durable Anti-fungal Resistance Processes in Cereals

Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene Lr34

Transcriptional profiling reveals no response of fungal pathogens to the durable, quantitative Lr34 disease resistance gene of wheat

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