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RNA-seq analysis provides insight into reprogramming of culm development in Zizania latifolia induced by Ustilago esculenta

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We report a transcriptome assembly and expression profiles from RNA-Seq data and identify genes responsible for culm gall formation in Zizania latifolia induced by Ustilago esculenta.

Abstract

The smut fungus Ustilago esculenta can induce culm gall in Zizania latifolia, which is used as a vegetable in Asian countries. However, the underlying molecular mechanism of culm gall formation is still unclear. To characterize the processes underlying this host-fungus association, we performed transcriptomic and expression profiling analyses of culms from Z. latifolia infected by the fungus U. esculenta. Transcriptomic analysis detected U. esculenta induced differential expression of 19,033 and 17,669 genes in Jiaobai (JB) and Huijiao (HJ) type of gall, respectively. Additionally, to detect the potential gall inducing genes, expression profiles of infected culms collected at −7, 1 and 10 DAS of culm gall development were  analyzed. Compared to control, we detected 8089 genes (4389 up-regulated, 3700 down-regulated) and 5251 genes (3121 up-regulated, 2130 down-regulated) were differentially expressed in JB and HJ, respectively. And we identified 376 host and 187 fungal candidate genes that showed stage-specific expression pattern, which are  possibly responsible for gall formation at the initial and later phases, respectively. Our results indicated that cytokinins play more prominent roles in regulating gall formation than do auxins. Together, our work provides general implications for the understanding of gene regulatory networks for culm gall development in Z. latifolia, and potential targets for genetic manipulation to improve the future yield   of  this crop.

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References

  • Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signalling in plant-microbe interactions. Science 276:726–733

    Article  CAS  PubMed  Google Scholar 

  • Balmer D, de Papajewski DV, Planchamp C, Glauser G, Mauch-Mani B (2013) Induced resistance in maize is based on organ-specific defence responses. Plant J 74:213–225

    Article  CAS  PubMed  Google Scholar 

  • Banuett F, Herskowitz I (1996) Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122:2965–2976

    CAS  PubMed  Google Scholar 

  • Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  CAS  PubMed  Google Scholar 

  • Basse CW, Lottspeich F, Steglich W, Kahmann R (1996) Two potential indole-3-acetaldehyde dehydrogenases in the phytopathogenic fungus Ustilago maydis. Eur J Biochem 242:648–656

    Article  CAS  PubMed  Google Scholar 

  • Bölker M, Basse CW, Schirawski J (2008) Ustilago maydis secondary metabolism-from genomics to biochemistry. Fungal Genet Biol 45:S88–S93

    Article  PubMed  Google Scholar 

  • Bruce SA, Saville BJ, Emery RJN (2011) Ustilago maydis produces cytokinins and abscisic acid for potential regulation of tumor formation in maize. J Plant Growth Regul 30:51–63

    Article  CAS  Google Scholar 

  • Chan YS, Thrower LB (1980a) The host-parasite relationship between Zizania caduciflora Turcz. and Ustilago esculenta P. Henn. I. Structure and development of the host and host-parasite combination. New Phytol 85:201–207

    Article  Google Scholar 

  • Chan YS, Thrower LB (1980b) The host-parasite relationship between Zizania caduciflora Turcz. and Ustilago esculenta P. Henn. IV. Growth substances in the host-parasite combination. New Phytol 85:225–233

    Article  Google Scholar 

  • Chung KR, Tzeng DD (2004) Biosynthesis of indole-3-acetic acid by the gall-inducing fungus Ustilago esculenta. J Biol Sci 4:744–750

    Article  CAS  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Crespi M, Messens E, Caplan AB, Van Montagu M, Desomer J (1992) Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene. EMBO J 11:795–804

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crespi M, Vereecke D, Temmerman W, Van Montagu M, Desomer J (1994) The fas operon of Rhodococcus fascians encodes new genes required for efficient fasciation of host plants. J Bacteriol 176:2492–2501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding XY, Xu XS, Chen WP (1991) A preliminary study on the development of “male” and smutted of Zizania caduciflora HAND.-MAZZ. J Wuhan Bot Res 9:115–123

    Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang L (2002) The phenylpropanoid pathway and plant defence: a genomics perspective. Mol Plant Pathol 3:371–390

    Article  CAS  PubMed  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548

    Article  CAS  PubMed  Google Scholar 

  • Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kühnemann J, Sonnewald U, Kahmann R, Kämper J (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56:181–195

    Article  CAS  PubMed  Google Scholar 

  • Doonan JH, Sablowski R (2010) Walls around tumours: why plants do not develop cancer. Nat Rev Cancer 10:794–802

    Article  CAS  PubMed  Google Scholar 

  • Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67:16–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo L, Qiu J, Han Z, Ye Z, Chen C, Liu C, Xin X, Ye CY, Wang YY, Xie H, Wang Y, Bao J, Tang S, Xu J, Gui Y, Fu F, Wang W, Zhang X, Zhu Q, Guang X, Wang C, Cui H, Cai D, Ge S, Tuskan GA, Yang X, Qian Q, He SY, Wang J, Zhou XP, Fan L (2015) A host plant genome (Zizania latifolia) after a century-long endophyte infection. Plant J 83:600–609

    Article  CAS  PubMed  Google Scholar 

  • Hahn M, Mendgen K (2001) Signal and nutrient exchange at biotrophic plant-fungus interfaces. Curr Opin Plant Biol 4:322–327

    Article  CAS  PubMed  Google Scholar 

  • Hemetsberger C, Herrberger C, Zechmann B, Hillmer M, Doehlemann G (2012) The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog 8:e1002684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horst RJ, Engelsdorf T, Sonnewald U, Voll LM (2008) Infection of maize leaves with Ustilago maydis prevents establishment of C4 photosynthesis. J Plant Physiol 165:19–28

    Article  CAS  PubMed  Google Scholar 

  • Jackson AO, Taylor CB (1996) Plant-microbe interactions: life and death at the interface. Plant Cell 8:1651–1668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Müller O, Perlin MH, Wösten HA, de Vries R, Ruiz-Herrera J, Reynaga-Peña CG, Snetselaar K, McCann M, Pérez-Martín J, Feldbrügge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, González-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Münch K, Rössel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Häuser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schlüter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Güldener U, Münsterkötter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101

    Article  PubMed  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Beisson F, Koo AJK, Molina I, Pollard M, Ohlrogge J (2007) Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA 104:18339–18344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li CY, Deng GM, Yang J, Viljoen A, Jin Y, Kuang RB, Zuo CW, Lv ZC, Yang QS, Sheng O, Wei YR, Hu CH, Dong T, Yi GJ (2012) Transcriptome profiling of resistant and susceptible Cavendish banana roots following inoculation with Fusarium oxysporum f. sp. cubense tropical race 4. BMC Genom 13:374

    Article  CAS  Google Scholar 

  • Lin Y, Lin C (1990) Involvement of tRNA bound cytokinin on the gall formation in Zizania. J Exp Bot 41:277–281

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

  • Lyons R, Stiller J, Powell J, Rusu A, Manners JM, Kazan K (2015) Fusarium oxysporum triggers tissue-specific transcriptional reprogramming in Arabidopsis thaliana. PLoS ONE 10:e0121902

    Article  PubMed  PubMed Central  Google Scholar 

  • Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2572–2853

    Article  Google Scholar 

  • Ménard R, Verdier G, Ors M, Erhardt M, Beisson F, Shen WH (2014) Histone H2B monoubiquitination is involved in the regulation of cutin and wax composition in Arabidopsis thaliana. Plant Cell Physiol 55:455–466

    Article  PubMed  Google Scholar 

  • Mendgen K, Hahn M (2002) Plant infection and the establishment of fungal biotrophy. Trends Plant Sci 7:352–356

    Article  CAS  PubMed  Google Scholar 

  • Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118

    Article  CAS  PubMed  Google Scholar 

  • Morrison EN, Emery RJN, Saville BJ (2015) Phytohormone involvement in the Ustilago maydis–Zea mays pathosystem: relationships between abscisic acid and cytokinin levels and strain virulence in infected cob tissue. PLoS One 10:e0130945

    Article  PubMed  PubMed Central  Google Scholar 

  • Nawrath C (2006) Unraveling the complex network of cuticular structure and function. Curr Opin Plant Biol 9:281–287

    Article  CAS  PubMed  Google Scholar 

  • Newton AC, Fitt BD, Atkins SD, Walters DR, Daniell TJ (2010) Pathogenesis, parasitism and mutualism in the trophic space of microbe-plant interactions. Trends Microbiol 18:365–373

    Article  CAS  PubMed  Google Scholar 

  • Rabe F, Ajami-Rashidi Z, Doehlemann G, Kahmann R, Djamei A (2013) Degradation of the plant defence hormone salicylic acid by the biotrophic fungus Ustilago maydis. Mol Microbiol 89:179–188

    Article  CAS  PubMed  Google Scholar 

  • Redkar A, Hoser R, Schilling L, Zechmann B, Krzymowska M, Walbot V, Doehlemann G (2015) A secreted effector protein of Ustilago maydis guides maize leaf cells to form tumors. Plant Cell 27:1332–1351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reineke G, Heinze B, Schirawski J, Buettner H, Kahmann R, Basse CW (2008) Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol Plant Pathol 9:339–355

    Article  CAS  PubMed  Google Scholar 

  • Robery PH, Fosket DE (1969) Changes in phenylalanine ammonia-lyase activity during xylem differentiation in Coleus and soybean. Planta 87:54–62

    Article  Google Scholar 

  • Rodríguez-Kessler M, Ruiz OA, Maiale S, Ruiz-Herrera J, Jiménez-Bremont JF (2008) Polyamine metabolism in maize tumors induced by Ustilago maydis. Plant Physiol Biochem 46:805–814

    Article  PubMed  Google Scholar 

  • Schlink K (2010) Down-regulation of defense genes and resource allocation into infected roots as factors for compatibility between Fagus sylvatica and Phytophthora citricola. Funct Integr Genom 10:253–264

    Article  CAS  Google Scholar 

  • Skibbe DS, Doehlemann G, Fernandes J, Walbot V (2010) Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328:89–92

    Article  CAS  PubMed  Google Scholar 

  • Tanaka S, Brefort T, Neidig N, Djamei A, Kahnt J, Vermerris W, Koenig S, Feussner K, Feussner I, Kahmann R (2014) A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. Elife 3:e01355

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang C, Qi J, Li H, Zhang C, Wang Y (2007) A convenient and efficient protocol for isolating high-quality RNA from latex of Hevea brasiliensis (para rubber tree). J Biochem Biophys Methods 70:749–754

    Article  CAS  PubMed  Google Scholar 

  • Tao Y, Xie Z, Chen W, Glazebrook J, Chang H, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Linde K, Hemetsberger C, Kastner C, Kaschani F, van der Hoorn RA, Kumlehn J, Doehlemann G (2012) A maize cystatin suppresses host immunity by inhibiting apoplastic cysteine proteases. Plant Cell 24:1285–1300

    Article  PubMed  PubMed Central  Google Scholar 

  • Wise RP, Moscou MJ, Bogdanove AJ, Whitham SA (2007) Transcript profiling in host-pathogen interactions. Annu Rev Phytopathol 45:329–369

    Article  CAS  PubMed  Google Scholar 

  • Wolf FT (1952) The production of indole acetic acid by Ustilago zeae, and its possible significance in tumor formation. Proc Natl Acad Sci USA 38:106–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan N, Wang XQ, Xu XF, Guo DP, Wang ZD, Zhang JZ, Hyde KD, Liu HL (2013a) Plant growth and photosynthetic performance of Zizania latifolia are altered by endophytic Ustilago esculenta infection. Physiol Mol Plant Pathol 83:75–83

    Article  CAS  Google Scholar 

  • Yan N, Xu XF, Wang ZD, Huang JZ, Guo DP (2013b) Interactive effects of temperature and light intensity on photosynthesis and antioxidant enzyme activity in Zizania latifolia Turcz. Photosynthetica 51:127–138

    Article  CAS  Google Scholar 

  • Yang HC, Leu LS (1978) Formation and histopathology of galls induced by Ustilago esculenta in Zizania latifolia. Phytopathology 68:1572–1576

    Article  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin Z, Ke X, Kang Z, Huang L (2016) Apple resistance responses against Valsa mali revealed by transcriptomics analyses. Physiol Mol Plant Pathol 93:85–92

    Article  CAS  Google Scholar 

  • You WY, Liu QA, Zou KQ, Yu XP, Cui HF, Ye ZH (2011) Morphological and molecular differences in two strains of Ustilago esculenta. Curr Microbiol 62:44–54

    Article  CAS  PubMed  Google Scholar 

  • Zhang JZ, Chu FQ, Hyde KD, Guo DP, Xie GL (2012) Cytology and ultrastructure of interactions between Ustilago esculenta and Zizania latifolia. Mycol Prog 11:499–508

    Article  CAS  Google Scholar 

  • Zhang JZ, Chu FQ, Guo DP, Ojaghian MR, Hyde KD (2014) The vacuoles containing multivesicularbodies: a new observation in interaction between Ustilago esculenta and Zizania latifolia. Eur J Plant Pathol 138:79–91

    Article  Google Scholar 

  • Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5:334–338

    Article  CAS  PubMed  Google Scholar 

  • Zuther K, Mayser P, Hettwer U, Wu W, Spiteller P, Kindler BL, Karlovsky P, Basse CW, Schirawski J (2008) The tryptophan aminotransferase Tam1 catalyses the single biosynthetic step for tryptophan-dependent pigment synthesis in Ustilago maydis. Mol Microbiol 68:152–172

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31372055 and 31571950).

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    Authors and Affiliations

    1. Department of Horticulture, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, China

      Zhi-Dan Wang, Ning Yan, Zheng-Hong Wang, Xiao-Huan Zhang, Hui-Min Xue, Li-Xia Wang, Qi Zhan, Ying-Ping Xu & De-Ping Guo

    2. Tobacco Research Institute of Chinese Academy of Agricultural Sciences, Qingdao, 266101, China

      Ning Yan

    3. Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, China

      Jing-Ze Zhang

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    1. Zhi-Dan Wang
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    2. Ning Yan
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    3. Zheng-Hong Wang
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    Contributions

    D-PG and J-ZZ conceived and designed the experiments. Z-DW and NY performed the experiments. Z-DW, NY, Z-HW, X-HZ, J-ZZ, H-MX, L-XW, QZ, Y-PX, and D-PG analysed the data. D-PG, Z-DW, and NY wrote the paper.

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    Correspondence to De-Ping Guo.

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    Zhi-Dan Wang and Ning Yan have contributed equally to this work and are co-first authors.

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    Wang, ZD., Yan, N., Wang, ZH. et al. RNA-seq analysis provides insight into reprogramming of culm development in Zizania latifolia induced by Ustilago esculenta . Plant Mol Biol 95, 533–547 (2017). https://doi.org/10.1007/s11103-017-0658-9

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