Resolving intergenotypic Striga resistance in sorghum

Genetic underpinnings of host-pathogen interactions in the parasitic plant Striga hermonthica,a root parasitic plant that ravages cereals in sub-Saharan Africa, are unclear. We performed a comparative transcriptome study on five genotypes of sorghum exhibiting diverse resistance responses to S. hermonthica using weighted gene co-expression network analysis (WGCNA). We found that S. hermonthica elicits both basal and effector-triggered immunity – like a bona fide pathogen. Resistance response was genotype-specific. Some resistance responses followed the salicylic acid-dependent signaling pathway for systemic acquired resistance characterized by cell wall reinforcements, lignification and callose deposition while in others the WRKY-dependent signaling pathway was activated leading to a hypersensitive response (HR). In some genotypes, both modes of resistance were activated while in others, either mode dominated the resistance response. Cell-wall-based resistance was common to all sorghum genotypes but strongest in IS2814, while HR-based response was specific to N13, IS9830 and IS41724. WGCNA further allowed for pinpointing of S. hermonthica resistance causative genes in sorghum. Some highlights include a Glucan synthase-like 10, a pathogenesis-related thaumatin-like family, and a phosphoinositide phosphatase gene. Such candidate genes will form a good basis for subsequent functional validation and possibly future resistance breeding. Highlight Parasitic plants of the Striga genus are major pests to cereals in Africa. We pinpointed genetic causes of Striga resistance in sorghum that can be harnessed for future resistance breeding.

[1]  Yuhan Tang,et al.  Melatonin enhances stem strength by increasing the lignin content and secondary cell wall thickness in herbaceous peony. , 2022, Journal of Experimental Botany.

[2]  J. Rodenburg,et al.  Combining host plant defence with targeted nutrition: key to durable control of hemi-parasitic Striga in cereals in sub-Saharan Africa? , 2021, The New phytologist.

[3]  M. Körner,et al.  A cell wall-localized glycine-rich protein of dodder acts as pathogen-associated molecular pattern , 2021, Communicative & Integrative Biology.

[4]  D. Odeny,et al.  GWAS provides biological insights into mechanisms of the parasitic plant (Striga) resistance in sorghum , 2020, BMC Plant Biology.

[5]  Runan Yao,et al.  ShinyGO: a graphical gene-set enrichment tool for animals and plants , 2019, Bioinform..

[6]  M. Timko,et al.  SHR4z, a novel decoy effector from the haustorium of the parasitic weed Striga gesnerioides, suppresses host plant immunity , 2019, The New phytologist.

[7]  Tetsuya Mori,et al.  The Structural Integrity of Lignin Is Crucial for Resistance against Striga hermonthica Parasitism in Rice1[OPEN] , 2019, Plant Physiology.

[8]  F. Kanampiu,et al.  Assessment of Management Options on Striga Infestation and Maize Grain Yield in Kenya , 2018, Weed Science.

[9]  A. Molina,et al.  Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. , 2018, The Plant journal : for cell and molecular biology.

[10]  S. Runo,et al.  Habits of a highly successful cereal killer, Striga , 2018, PLoS pathogens.

[11]  C. Zipfel,et al.  Cellulose-Derived Oligomers Act as Damage-Associated Molecular Patterns and Trigger Defense-Like Responses1 , 2017, Plant Physiology.

[12]  M. Timko,et al.  Novel Sources of Witchweed (Striga) Resistance from Wild Sorghum Accessions , 2017, Front. Plant Sci..

[13]  Daniel I Bolnick,et al.  Evaluation of TagSeq, a reliable low‐cost alternative for RNAseq , 2016, Molecular ecology resources.

[14]  Daniel MacLean,et al.  bio-samtools 2: a package for analysis and visualization of sequence and alignment data with SAMtools in Ruby , 2015, Bioinform..

[15]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[16]  S. Salzberg,et al.  StringTie enables improved reconstruction of a transcriptome from RNA-seq reads , 2015, Nature Biotechnology.

[17]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[18]  Patrick Schweizer,et al.  Differential accumulation of callose, arabinoxylan and cellulose in nonpenetrated versus penetrated papillae on leaves of barley infected with Blumeria graminis f. sp. hordei. , 2014, The New phytologist.

[19]  Imara Y. Perera,et al.  Phosphoinositide-signaling is one component of a robust plant defense response , 2014, Front. Plant Sci..

[20]  C. Voigt.  Callose-mediated resistance to pathogenic intruders in plant defense-related papillae , 2014, Front. Plant Sci..

[21]  Anil Kumar Singh,et al.  Overexpression of Camellia sinensis Thaumatin-Like Protein, CsTLP in Potato Confers Enhanced Resistance to Macrophomina phaseolina and Phytophthora infestans Infection , 2013, Molecular Biotechnology.

[22]  S. Somerville,et al.  Elevated Early Callose Deposition Results in Complete Penetration Resistance to Powdery Mildew in Arabidopsis1[C][W][OA] , 2013, Plant Physiology.

[23]  A. Mackey,et al.  Global changes in gene expression during compatible and incompatible interactions of cowpea (Vigna unguiculata L.) with the root parasitic angiosperm Striga gesnerioides , 2012, BMC Genomics.

[24]  P. Ronald,et al.  Plant innate immunity: perception of conserved microbial signatures. , 2012, Annual review of plant biology.

[25]  Xin He,et al.  Molecular cloning of a thaumatin-like protein gene from Pyrus pyrifolia and overexpression of this gene in tobacco increased resistance to pathogenic fungi , 2012, Plant Cell, Tissue and Organ Culture (PCTOC).

[26]  M. Matz,et al.  Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA‐Seq procedure , 2011, Molecular ecology.

[27]  Chung-Mo Park,et al.  Expression of Arabidopsis pathogenesis-related genes during nematode infection. , 2011, Molecular plant pathology.

[28]  Harro Bouwmeester,et al.  Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. , 2011, Journal of plant physiology.

[29]  S. Duplessis,et al.  Genome-wide analysis of eukaryote thaumatin-like proteins (TLPs) with an emphasis on poplar , 2011, BMC Plant Biology.

[30]  Mark D. Robinson,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[31]  M. Timko,et al.  Molecular genetics of race-specific resistance of cowpea to Striga gesnerioides (Willd.). , 2009, Pest management science.

[32]  Steve Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[33]  Jean-Charles Portais,et al.  Strigolactone inhibition of shoot branching , 2008, Nature.

[34]  J. Slate,et al.  Global patterns of gene expression in rice cultivars undergoing a susceptible or resistant interaction with the parasitic plant Striga hermonthica. , 2008, The New phytologist.

[35]  Y. Sugimoto,et al.  Molecular Responses of Sorghum to Purple Witchweed (Striga hermonthica) Parasitism , 2008, Weed Science.

[36]  G. Ejeta.  THE STRIGA SCOURGE IN AFRICA: A GROWING PANDEMIC , 2007 .

[37]  H. Bouwmeester,et al.  Rhizosphere communication of plants, parasitic plants and AM fungi. , 2007, Trends in plant science.

[38]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[39]  H. Bouwmeester,et al.  The Strigolactone Germination Stimulants of the Plant-Parasitic Striga and Orobanche spp. Are Derived from the Carotenoid Pathway1 , 2005, Plant Physiology.

[40]  B. Reddy,et al.  Genomic regions influencing resistance to the parasitic weed Striga hermonthica in two recombinant inbred populations of sorghum , 2004, Theoretical and Applied Genetics.

[41]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[42]  Nicolai Strizhov,et al.  An Arabidopsis Callose Synthase, GSL5, Is Required for Wound and Papillary Callose Formation Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016097. , 2003, The Plant Cell Online.

[43]  Imara Y. Perera,et al.  Inositol signaling and plant growth , 2000, Trends in plant science.

[44]  I. Dörr.  How Striga Parasitizes its Host: a TEM and SEM Study , 1997 .

[45]  K. Ramaiah,et al.  A Comparative Study of the Haustorial Development of Striga asiatica (L.) Kuntze on Sorghum Cultivars , 1984 .

[46]  J. Doe.  Sand and Water Culture Methods Used in the Study of Plant Nutrition , 1953, Soil Science Society of America Journal.

[47]  L.,et al.  Plant Cell, Tissue and Organ Culture (PCTOC) , 2017 .

[48]  S. Yoshida,et al.  The WRKY 45-Dependent Signaling Pathway Is Required For Resistance against Striga hermonthica Parasitism 1 [ OPEN ] , 2015 .

[49]  D. Berner,et al.  Striga research and control: a perspective from Africa , 1995 .