ANTHRACNOSE RESISTANCE GENE2 confers fungal resistance in sorghum

Sorghum is an important food and feed crop globally; its production is hampered by anthracnose disease caused by the fungal pathogen Colletotrichum sublineola (Cs). Here, we report identification and characterization of ANTHRACNOSE RESISTANCE GENE 2 (ARG2) encoding a nucleotide-binding leucine-rich repeat (NLR) protein that confers race-specific resistance to Cs strains. ARG2 is one of a cluster of several NLR genes in the sorghum differential line SC328C that is resistant to some Cs strains. This cluster shows structural and copy number variations in different sorghum genotypes. Different sorghum variants carrying independent ARG2 alleles provided the genetic validation for the identity of the ARG2 gene. ARG2 expression is induced by Cs, and chitin induce ARG2 expression in resistant but not in susceptible lines. ARG2-mediated resistance is accompanied by higher expression of defense and secondary metabolite genes at early stages of infection, and anthocyanin and zeatin metabolisms are upregulated in resistant plants. Interestingly, ARG2 localizes to the plasma membrane when transiently expressed in Nicotiana benthamiana. Importantly, ARG2 plants produced higher shoot dry matter than near-isogenic lines carrying the susceptible allele suggesting absence of an ARG2 associated growth trade-off. Further, ARG2-mediated resistance is stable at a wide range of temperatures. Our observations open avenues for resistance breeding and for dissecting mechanisms of resistance.

[1]  F. Fu,et al.  Broad-spectrum fungal resistance in sorghum is conferred through the complex regulation of an immune receptor gene embedded in a natural antisense transcript , 2022, The Plant cell.

[2]  Farid El Kasmi.  How activated NLRs induce anti-microbial defenses in plants , 2021, Biochemical Society transactions.

[3]  S. Kamoun,et al.  RefPlantNLR is a comprehensive collection of experimentally validated plant disease resistance proteins from the NLR family , 2021, PLoS biology.

[4]  P. Staswick,et al.  PhenoImage: An open‐source graphical user interface for plant image analysis , 2021, The Plant Phenome Journal.

[5]  F. Fu,et al.  Global mRNA and microRNA expression dynamics in response to anthracnose infection in sorghum , 2020, BMC Genomics.

[6]  U. Nagalakshmi,et al.  Plant NLR immune receptor Tm-22 activation requires NB-ARC domain-mediated self-association of CC domain , 2020, PLoS pathogens.

[7]  Jonathan D. G. Jones,et al.  A Species-Wide Inventory of NLR Genes and Alleles in Arabidopsis thaliana , 2019, Cell.

[8]  S. Shu,et al.  A new reference genome for Sorghum bicolor reveals high levels of sequence similarity between sweet and grain genotypes: implications for the genetics of sugar metabolism , 2019, BMC Genomics.

[9]  S. Whitham,et al.  Engineering a Decoy Substrate in Soybean to Enable Recognition of the Soybean Mosaic Virus NIa Protease , 2018, bioRxiv.

[10]  Y. Qi,et al.  Reconstitution and structure of a plant NLR resistosome conferring immunity , 2019, Science.

[11]  Larry Lambright.  Hybrid Sorghum Product Development and Production. , 2019, Methods in molecular biology.

[12]  G. Doehlemann,et al.  Visualization of Growth and Morphology of Fungal Hyphae in planta Using WGA-AF488 and Propidium Iodide Co-staining , 2018 .

[13]  Tyr Wiesner-Hanks,et al.  Navigating complexity to breed disease-resistant crops , 2017, Nature Reviews Genetics.

[14]  Zonghua Wang,et al.  The arms race between Magnaporthe oryzae and rice: Diversity and interaction of Avr and R genes , 2017 .

[15]  P. Klein,et al.  Quantitative Trait Loci Associated with Anthracnose Resistance in Sorghum , 2017 .

[16]  METHODS AND COMPOSITIONS FOR PRODUCING SORGHUM PLANTS WITH ANTHRACNOSE RESISTANCE , 2017 .

[17]  Rukmini Mishra,et al.  Differential expression of defense-related genes in chilli pepper infected with anthracnose pathogen Colletotrichum truncatum , 2017 .

[18]  C. Gilligan,et al.  Trade-off between disease resistance and crop yield: a landscape-scale mathematical modelling perspective , 2016, Journal of The Royal Society Interface.

[19]  W. Vermerris,et al.  Using Genotyping by Sequencing to Map Two Novel Anthracnose Resistance Loci in Sorghum bicolor , 2016, G3: Genes, Genomes, Genetics.

[20]  L. Mur,et al.  Senescence and programmed cell death , 2015 .

[21]  Michael J E Sternberg,et al.  The Phyre2 web portal for protein modeling, prediction and analysis , 2015, Nature Protocols.

[22]  J. Parker,et al.  Effector-triggered immunity: from pathogen perception to robust defense. , 2015, Annual review of plant biology.

[23]  P. Klein,et al.  Sequencing of an Anthracnose‐Resistant Sorghum Genotype and Mapping of a Major QTL Reveal Strong Candidate Genes for Anthracnose Resistance , 2015 .

[24]  H. Cuevas,et al.  Inheritance and molecular mapping of anthracnose resistance genes present in sorghum line SC112-14 , 2014, Molecular Breeding.

[25]  Xin Li,et al.  Arabidopsis HSP90 protein modulates RPP4-mediated temperature-dependent cell death and defense responses. , 2014, The New phytologist.

[26]  Blockin Blockin,et al.  New whole genome de novo assemblies of three divergent strains of rice ( O. sativa ) documents novel gene space of aus and indica , 2014 .

[27]  R. Terauchi,et al.  QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. , 2013, The Plant journal : for cell and molecular biology.

[28]  J. Rathjen,et al.  Recognition and Response in Plant PAMP‐Triggered Immunity , 2012 .

[29]  S. Ramachandran,et al.  Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor) , 2011, Genome Biology.

[30]  B. Kobe,et al.  An autoactive mutant of the M flax rust resistance protein has a preference for binding ATP, whereas wild-type M protein binds ADP. , 2011, Molecular plant-microbe interactions : MPMI.

[31]  W. Rooney,et al.  Evaluation of bioethanol production from five different varieties of sweet and forage sorghums (Sorghum bicolor (L) Moench) , 2011 .

[32]  D. S. St. Clair,et al.  Quantitative disease resistance and quantitative resistance Loci in breeding. , 2010, Annual review of phytopathology.

[33]  Yexiong Qian,et al.  A genomic analysis of disease-resistance genes encoding nucleotide binding sites in Sorghum bicolor , 2010, Genetics and molecular biology.

[34]  Yang Zhang,et al.  I-TASSER: a unified platform for automated protein structure and function prediction , 2010, Nature Protocols.

[35]  D. TeBeest,et al.  Pathotypes of Colletotrichum sublineolum in Arkansas. , 2008, Plant disease.

[36]  M. Albrecht,et al.  Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. , 2008, Journal of experimental botany.

[37]  R. Thakur.  Genetic resistance to foliar anthracnose in sorghum and pathogenic variability in Colletotrichum graminicola , 2007 .

[38]  R. Michelmore,et al.  The Maintenance of Extreme Amino Acid Diversity at the Disease Resistance Gene, RPP13, in Arabidopsis thaliana , 2004, Genetics.

[39]  J. Vossen,et al.  The Tomato R Gene Products I-2 and Mi-1 Are Functional ATP Binding Proteins with ATPase Activity , 2002, The Plant Cell Online.

[40]  R. Nicholson,et al.  Accumulation of 3-deoxyanthocyanidin phytoalexins and resistance to Colletotrichum sublineolum in sorghum , 1999 .

[41]  R. Nicholson,et al.  cDNA cloning of a sorghum pathogenesis-related protein (PR-10) and differential expression of defense-related genes following inoculation with Cochliobolus heterostrophus or Colletotrichum sublineolum. , 1999, Molecular plant-microbe interactions : MPMI.

[42]  Hiroyuki Ogata,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 1999, Nucleic Acids Res..

[43]  J. Dangl,et al.  The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[44]  F. Miller,et al.  Phytoalexin Assay in Juvenile Sorghum: An Aid to Breeding for Anthracnose Resistance , 1993 .

[45]  R. Nicholson,et al.  Susceptibility of corn to isolates of Colletotrichum graminicola pathogenic to other grasses. , 1987 .