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Transcriptional profiling of underground interaction of two contrasting sunflower cultivars with the root parasitic weed Orobanche cumana

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Abstract

Aims

Orobanche cumana is an obligate root parasite which specifically infects roots of Helianthus annuus L., causing severe yield and economic losses in agricultural fields worldwide. For an efficient control strategy, it is necessary to understand specialized host defense mechanisms and the pathogenesis of O. cumana during underground interaction with the host.

Methods

RNA-Seq was used to simultaneously assess the transcriptome of each of two contrasting sunflower cultivars with O. cumana during their post-attachment interactions. Secretome prediction was applied to identify O. cumana proteins from its transcriptome.

Results

Infection of O. cumana triggered insufficient defense responses in the susceptible cultivar as compared to the resistant one, probably due to the failure to fully recognize parasite effectors. Secretome prediction from the O. cumana transcriptome enabled robust identification of 180 proteins associated with O. cumana penetration and infection. Functional annotation of these proteins revealed that they were associated with cell wall degradation, nutrient acquisition and pathogenesis. Additionally, a candidate effector containing a PAR1 domain from O. cumana was preliminarily identified as a potential suppressor of plant defense responses.

Conclusions

Secretome prediction shed lights on the molecular mechanisms that O. cumana deployed to manipulate host defense. Successful infection of O. cumana inhibited host defense responses and turned host roots from a sink to a source for efficient nutrient flux towards the parasite. In summary, these findings provide insight into the mechanism underlying O. cumana infection and are important in understanding parasitic-host plant interaction.

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References

  • Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot 58:4019–4026

    Article  CAS  PubMed  Google Scholar 

  • Cameron DD, Coats AM, Seel WE (2006) Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor. Ann Bot 98:1289–1299

    Article  PubMed  PubMed Central  Google Scholar 

  • Clarke CR, Chinchilla D, Hind SR, Taguchi F, Miki R, Ichinose Y, Martin GB, Leman S, Felix G, Vinatzer BA (2013) Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytol 200:847–860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daniel-Vedele F, Filleur S, Caboche M (1998) Nitrate transport: a key step in nitrate assimilation. Curr Opin Plant Biol 1:235–239

    Article  CAS  PubMed  Google Scholar 

  • de Zelicourt A, Letousey P, Thoiron S, Campion C, Simoneau P, Elmorjani K, Marion D, Simier P, Delavault P (2007) Ha-DEF1, a sunflower defensin, induces cell death in Orobanche parasitic plants. Planta 226:591–600

    Article  CAS  PubMed  Google Scholar 

  • Díaz-Sánchez J, Jurado-Expósito M, López-Granados F, Castejón-Muñoz M, García-Torres L (2003) Pronamide applied to sunflower seeds for Orobanche cumana control. Weed Technol 17:314–319

  • Echevarria-Zomeno S, Perez-de-Luque A, Jorrin J, Maldonado AM (2006) Pre-haustorial resistance to broomrape (Orobanche cumana) in sunflower (Helianthus annuus): cytochemical studies. J Exp Bot 57:4189–4200

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, Heijne GV (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  CAS  PubMed  Google Scholar 

  • Faik A, Abouzouhair J, Sarhan F (2006) Putative fasciclin-like arabinogalactan-proteins (FLA) in wheat (Triticum aestivum) and rice (Oryza sativa): identification and bioinformatic analyses. Mol Gen Genomics 276:478–494

    Article  CAS  Google Scholar 

  • Fatima U, Senthil-Kumar M (2015) Plant and pathogen nutrient acquisition strategies. Front Plant Sci 6:750

    Article  PubMed  PubMed Central  Google Scholar 

  • Guyon K, Balagué C, Roby D, Raffaele S (2014) Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum. BMC Genomics 15:336

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512

    Article  CAS  PubMed  Google Scholar 

  • Hématy K, Cherk C, Somerville S (2009) Host-pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12:406–413

  • Herbers K, Mönke G, Badur R, Sonnewald U (1995) A simplified procedure for the subtractive cDNA cloning of photoassimilate-responding genes: isolation of cDNAs encoding a new class of pathogenesis-related proteins. Plant Mol Biol 29:1027–1038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Honaas LA, Wafula EK, Yang ZZ, Der JP, Wickett NJ, Altman NS, Taylor CG, Yoder JI, Timko MP, Westwood JH, dePamphilis CW (2013) Functional genomics of a generalist parasitic plant: laser microdissection of host-parasite interface reveals host-specific patterns of parasite gene expression. BMC Plant Biol 13:9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huckelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45:101–127

    Article  PubMed  CAS  Google Scholar 

  • Jacobs JM, Babujee L, Meng F, Milling A, Allen C (2012) The in planta transcriptome of Ralstonia solanacearum: conserved physiological and virulence strategies during bacterial wilt of tomato MBio 3

  • Joel DM (2000) The long-term approach to parasitic weeds control: manipulation of specific developmental mechanisms of the parasite. Crop Prot 19:753–758

    Article  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    CAS  PubMed  Google Scholar 

  • Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447–463

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim G, LeBlanc ML, Wafula EK, dePamphilis CW, Westwood JH (2014) Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345:808

    Article  CAS  PubMed  Google Scholar 

  • Labrousse P, Arnaud MC, Serieys H, Bervillé A, Thalouarn P (2001) Several mechanisms are involved in resistance of Helianthus to Orobanche cumana Wallr. Ann Bot 88:859–868

    Article  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Letousey P, De Zélicourt A, Vieira Dos Santos C, Thoiron S, Monteau F, Simier P, Thalouarn P, Delavault P (2007) Molecular analysis of resistance mechanisms to Orobanche cumana in sunflower. Plant Pathol 56:536–546

    Article  CAS  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Jaroszewski L, Godzik A (2002) Tolerating some redundancy significantly speeds up clustering of large protein databases. Bioinformatics 18:77–82

    Article  CAS  PubMed  Google Scholar 

  • Li J, Yang C, Liu H, Cao M, Yan G, Si P, Zhou W, Xu L (2019) 5-aminolevolinic acid enhances sunflower resistance to Orobanche cumana (broomrape). Ind Crop Prod 140:111467

    Article  CAS  Google Scholar 

  • Liu N, Shen GJ, Xu YX, Liu H, Zhang JX, Li SL, Li J, Zhang CP, Qi JF, Wang L, Wu JQ (2019) Extensive inter-plant protein transfer between Cuscuta parasites and their host plants. Mol Plant doi. https://doi.org/10.1016/j.molp.2019.12.002

  • Louarn J, Boniface MC, Pouilly N, Velasco L, Perez-Vich B, Vincourt P, Munos S (2016) Sunflower resistance to broomrape (Orobanche cumana) is controlled by specific QTLs for different parasitism stages. Front Plant Sci 7:590

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch TM, Lintilhac PM (1997) Mechanical signals in plant development: a new method for single cell studies. Dev Biol 181:246–256

    Article  CAS  PubMed  Google Scholar 

  • Molinero-Ruiz ML, Melero-Vara JM, GarcÍA-Ruiz R, DomÍNguez J (2006) Pathogenic diversity within field populations of Orobanche cumana and different reactions on sunflower genotypes. Weed Res 46:462–469

  • Molinero-Ruiz L, García-Carneros AB, Collado-Romero M, Raranciuc S, Domínguez J, Melero-Vara JM, Vurro M (2014) Pathogenic and molecular diversity in highly virulent populations of the parasitic weed Orobanche cumana (sunflower broomrape) from Europe. Weed Res 54:87–96

    Article  Google Scholar 

  • Molinero-Ruiz L, Delavault P, Pérez-Vich B, Pacureanu-Joita M, Bulos M, Altieri E, Domínguez J (2015) History of the race structure of Orobanche cumana and the breeding of sunflower for resistance to this parasitic weed: a review. Span J Agric Res 13:e10R01

    Article  Google Scholar 

  • Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15:349–357

  • Müller-Stöver D, Thomas H, Sauerborn J, Kroschel J (2004) Two granular formulations of Fusarium oxysporum f.sp. orthoceras to mitigate sunflower broomrape Orobanche cumana. Biocontrol 49:595–602

  • Nabloussi A, Velasco L, Assissel N (2017) First report of sunflower broomrape, Orobanche cumana Wallr. In Morocco. Plant Dis 102:457–457

    Article  Google Scholar 

  • Nakagawa T, Ishiguro S, Kimura T (2009) Gateway vectors for plant transformation. Plant Biotech 26:275–284

    Article  CAS  Google Scholar 

  • O'Connell RJ, Thon MR, Hacquard S (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44:1060–1065

    Article  CAS  PubMed  Google Scholar 

  • Pedersen C, van Themaat EVL, McGuffin LJ, Abbott JC, Burgis TA, Barton G, Bindschedler LV, Lu X, Maekawa T, Weßling R, Cramer R, Thordal-Christensen H, Panstruga R, Spanu PD (2012) Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13:694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen TN, Brunak S, Heijne GV, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  CAS  PubMed  Google Scholar 

  • Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R, Couloux A, Darrasse A, Gouzy J, Jacques M-A, Lauber E, Manceau C, Mangenot S, Poussier S, Segurens B, Szurek B, Verdier V, Arlat M, Gabriel DW, Rott P, Cociancich S (2012) Genomic insights into strategies used by Xanthomonas albilineans with its reduced artillery to spread within sugarcane xylem vessels. BMC Genomics 13:658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pineda-Martos R, Velasco L, Pérez-Vich B, Iannetta P (2014) Identification, characterisation and discriminatory power of microsatellite markers in the parasitic weed Orobanche cumana. Weed Res 54:120–132

    Article  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. BBA-Bioenergetics 975:384–394

    Article  CAS  Google Scholar 

  • Qin L, Kudla U, Roze EHA, Goverse A, Popeijus H, Nieuwland J, Overmars H, Jones JT, Schots A, Smant G, Bakker J, Helder J (2004) A nematode expansin acting on plants. Nature 427:30

    Article  CAS  PubMed  Google Scholar 

  • Raupp FM, Spring O (2013) New sesquiterpene lactones from sunflower root exudate as germination stimulants for Orobanche cumana. J Agric Food Chem 61:10481–10487

    Article  CAS  PubMed  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    CAS  PubMed  Google Scholar 

  • Rodenburg J, Riches CR, Kayeke JM (2010) Addressing current and future problems of parasitic weeds in rice. Crop Prot 29:210–221

    Article  Google Scholar 

  • Rubiales D, Fernandez-Aparicio M, Perez-de-Luque A, Castillejo MA, Prats E, Sillero JC, Rispail N, Fondevilla S (2009) Breeding approaches for crenate broomrape (Orobanche crenata Forsk.) management in pea (Pisum sativum L.). Pest Manag Sci 65:553–559

    Article  CAS  PubMed  Google Scholar 

  • Scholes JD, Press MC (2008) Striga infestation of cereal crops - an unsolved problem in resource limited agriculture. Curr Opin Plant Biol 11:180–186

    Article  PubMed  Google Scholar 

  • Sestacova T, Giscă I, Cucereavîi A, Port A, Duca M (2016) Expression of defence-related genes in sunflower infected with broomrape. Biotechnol Biotech Eq 30:685–691

    Article  CAS  Google Scholar 

  • Shahid S, Kim G, Johnson NR, Wafula E, Wang F, Coruh C, Bernal-Galeano V, Phifer T, dePamphilis CW, Westwood JH, Axtell MJ (2018) MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 553:82–85

    Article  CAS  PubMed  Google Scholar 

  • Shi BX, Chen GH, Zhang ZJ, Hao JJ, Jing L, Zhou HY, Zhao J (2015) First report of race composition and distribution of sunflower broomrape, Orobanche cumana, in China. Plant Dis 99:291

    Article  CAS  PubMed  Google Scholar 

  • Song WJ, Cao DD, Jin ZL, Zhang D (2005a) The host, damage and control of root parasitic plant Orobanche in China. Plant Quarantine 19:230–232

    Google Scholar 

  • Song WJ, Zhou WJ, Jin ZL, Cao DD, Joel DM, Takeuchi Y, Yoneyama K (2005b) Germination response of Orobanche seeds subjected to conditioning temperature, water potential and growth regulator treatments. Weed Res 45:467–476

    Article  Google Scholar 

  • Ueno K, Furumoto T, Umeda S, Mizutani M, Takikawa H, Batchvarova R, Sugimoto Y (2014) Heliolactone, a non-sesquiterpene lactone germination stimulant for root parasitic weeds from sunflower. Phytochemistry 108:122–128

    Article  CAS  PubMed  Google Scholar 

  • Velasco L, Pérez-Vich B, Yassein AAM, Jan CC, Fernández-Martínez JM (2012) Inheritance of resistance to sunflower broomrape (Orobanche cumana Wallr.) in an interspecific cross between Helianthus annuus and Helianthus debilis subsp. tardiflorus. Plant Breed 131:220–221

    Article  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants – protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Yang Z, Wafula EK, Honaas LA, Zhang H, Das M, Fernandez-Aparicio M, Huang K, Bandaranayake PC, Wu B, Der JP, Clarke CR, Ralph PE, Landherr L, Altman NS, Timko MP, Yoder JI, Westwood JH, dePamphilis CW (2015) Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty. Mol Biol Evol 32:767–790

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Hu LY, Ali B, Islam F, Bai QJ, Yun XP, Yoneyama K, Zhou WJ (2016) Seed treatment with salicylic acid invokes defence mechanism of Helianthus annuus against Orobanche cumana. Ann Appl Biol 169:408–422

    Article  CAS  Google Scholar 

  • Yang C, Xu L, Zhang N, Islam F, Song W, Hu L, Liu D, Xie X, Zhou W (2017) iTRAQ-based proteomics of sunflower cultivars differing in resistance to parasitic weed Orobanche cumana. Proteomics 17:1700009

  • Zhou W, Leul M (1998) Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regul 26:41–47

    Article  CAS  Google Scholar 

  • Zhou WJ, Yoneyama K, Takeuchi Y, Iso S, Rungmekarat S, Chae SH, Sato D, Joel DM (2004) In vitro infection of host roots by differentiated calli of the parasitic plant Orobanche. J Exp Bot 55:899–907

    Article  CAS  PubMed  Google Scholar 

  • Zipfel C, Robatzek S (2010) Pathogen-associated molecular pattern-triggered immunity: veni, vidi...? Plant Physiol 154:551–554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (31701333, 31570434), GDAS’ Project of Science and Technology Development (2020GDASYL-20200103062), National Special Oil Crops Industry Technology System (CARS-14-1-21), Inner Mongolia Science & Technology Plan (201802072), the Science and Technology Department of Zhejiang Province (2016C02050-8, LGN18C130007), and Jiangsu Collaborative Innovation Center for Modern Crop Production.

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  1. Chong Yang and Fei Fu contributed equally to this work.

Authors and Affiliations

  1. Bioengineering Research Laboratory, Guangdong Bioengineering Institute (Guangzhou Sugarcane Industry Research Institute), Guangzhou, China

    Chong Yang

  2. Institute of Crop Science and Zhejiang Key Lab of Crop Germplasm, Zhejiang University, Hangzhou, China

    Chong Yang, Fei Fu, Na Zhang, Jiansu Wang, Luyang Hu, Faisal Islam & Weijun Zhou

  3. Institute of Plant Protection, Inner Mongolia Academy of Agricultural and Animal Husbandry Sciences, Hohhot, China

    Quanjiang Bai & Xiaopeng Yun

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  1. Chong Yang
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Correspondence to Weijun Zhou.

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Yang, C., Fu, F., Zhang, N. et al. Transcriptional profiling of underground interaction of two contrasting sunflower cultivars with the root parasitic weed Orobanche cumana. Plant Soil 450, 303–321 (2020). https://doi.org/10.1007/s11104-020-04495-3

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