Abstract
Waterlogging is a severe abiotic stressor that inhibits crop growth and productivity owing to the decline in the amount of oxygen available to the waterlogged organs. Although melon (Cucumis melo L.) is sensitive to waterlogging, its ability to form adventitious roots facilitates the diffusion of oxygen and allows the plant to survive waterlogging. To provide comprehensive insight into the adventitious rooting in response to waterlogging of melon, global transcriptome changes during this process were investigated. Of the 17,146 genes expressed during waterlogging, 7363 of them were differentially expressed in the pairwise comparisons between different waterlogging treatment time points. A further analysis suggested that the genes involved in sugar cleavage, glycolysis, fermentation, reactive oxygen species scavenging, cell wall modification, cell cycle governing, microtubule remodeling, hormone signals and transcription factors could play crucial roles in the adventitious root production induced by waterlogging. Additionally, ethylene and ERFs were found to be vital factors that function in melon during adventitious rooting. This study broadens our understanding of the mechanisms that underlie adventitious rooting induced by waterlogging and lays the theoretical foundation for further molecular breeding of waterlogging-tolerant melon.
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All datasets obtained in this study are included in the manuscript and supplementary data.
References
Abu-Abied M, Szwerdszarf D, Mordehaev I, Yaniv Y, Levinkron S, Rubinstein M, Riov J, Ophir R, Sadot E (2014) Gene expression profiling in juvenile and mature cuttings of Eucalyptus grandis reveals the importance of microtubule remodeling during adventitious root formation. BMC Genomics 15:826. https://doi.org/10.1186/1471-2164-15-826
Abu-Abied M, Mordehaev I, Sunil Kumar GB, Ophir R, Wasteneys GO, Sadot E (2015) Analysis of microtubule-associated-proteins during IBA-mediated adventitious root induction reveals KATANIN dependent and independent alterations of expression patterns. PLoS ONE 10(12):e0143828. https://doi.org/10.1371/journal.pone.0143828
Alexa A, Rahnenfuhrer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22(13):1600–1607. https://doi.org/10.1093/bioinformatics/btl140
Bailey-Serres J, Voesenek LA (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339. https://doi.org/10.1146/annurev.arplant.59.032607.092752
Boru G, Vantoai T, Alves J, Hua D, Knee M (2003) Responses of soybean to oxygen deficiency and elevated root-zone carbon dioxide concentration. Ann Bot 91(4):447–453. https://doi.org/10.1093/aob/mcg040
Burger Y, Sa’ar U, Paris H, Lewinsohn E, Katzir N, Tadmor Y, Schaffer A (2006) Genetic variability for valuable fruit quality traits in Cucumis melo. Isr J Plant Sci 54(3):233–242. https://doi.org/10.1560/ijps_54_3_233
Calvo-Polanco M, Senorans J, Zwiazek JJ (2012) Role of adventitious roots in water relations of tamarack (Larix laricina) seedlings exposed to flooding. BMC Plant Biol 12:99. https://doi.org/10.1186/1471-2229-12-99
Dawood T, Rieu I, Wolters-Arts M, Derksen EB, Mariani C, Visser EJW (2014) Rapid flooding-induced adventitious root development from preformed primordia in Solanum dulcamara. Aob Plants. https://doi.org/10.1093/aobpla/plt058
Dawood T, Yang X, Visser EJW, te Beek TAH, Kensche PR, Cristescu SM, Lee S, Floková K, Nguyen D, Mariani C, Rieu I (2016) A Co-Opted Hormonal Cascade Activates Dormant Adventitious Root Primordia upon Flooding in Solanum dulcamara. Plant Physiol 170(4):2351–2364. https://doi.org/10.1104/pp.15.00773
Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, Murray JAH (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. P Natl Acad Sci USA 104(36):14537–14542. https://doi.org/10.1073/pnas.0704166104
Dong CJ, Li L, Shang QM, Liu XY, Zhang ZG (2014) Endogenous salicylic acid accumulation is required for chilling tolerance in cucumber (Cucumis sativus L.) seedlings. Planta 240(4):687–700. https://doi.org/10.1007/s00425-014-2115-1
Ernst J, Bar-Joseph Z (2006) STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 7:191. https://doi.org/10.1186/1471-2105-7-191
Gibbs DJ, Conde JV, Berckhan S, Prasad G, Mendiondo GM, Holdsworth MJ (2015) Group VII ethylene response factors coordinate oxygen and nitric oxide signal transduction and stress responses in plants. Plant Physiol 169(1):23–31. https://doi.org/10.1104/pp.15.00338
Guénin S, Mareck A, Rayon C, Lamour R, Assoumou Ndong Y, Domon J-M, Sénéchal F, Fournet F, Jamet E, Canut H, Percoco G, Mouille G, Rolland A, Rustérucci C, Guerineau F, Van Wuytswinkel O, Gillet F, Driouich A, Lerouge P, Gutierrez L, Pelloux J (2011) Identification of pectin methylesterase 3 as a basic pectin methylesterase isoform involved in adventitious rooting in Arabidopsis thaliana. New Phytol 192(1):114–126. https://doi.org/10.1111/j.1469-8137.2011.03797.x
Gutierrez L, Mongelard G, Floková K, Păcurar DI, Novák O, Staswick P, Kowalczyk M, Păcurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24(6):2515–2527. https://doi.org/10.1105/tpc.112.099119
Hao D, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plant. J Biol Chem 273(41):26857–26861. https://doi.org/10.1074/jbc.273.41.26857
Hermann K, Meinhard J, Dobrev P, Linkies A, Pesek B, Heß B, Macháčková I, Fischer U, Leubner-Metzger G (2007) 1-Aminocyclopropane-1-carboxylic acid and abscisic acid during the germination of sugar beet (Beta vulgaris L.): a comparative study of fruits and seeds. J Exp Bot 58(11):3047–3060. https://doi.org/10.1093/jxb/erm162
Hinz M, Wilson IW, Yang J, Buerstenbinder K, Llewellyn D, Dennis ES, Sauter M, Dolferus R (2010) Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol 153(2):757–772
Houston K, Tucker MR, Chowdhury J, Shirley N, Little A (2016) The plant cell wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00984
Jackson MB (1985) Ethylene and responses of plants to soil waterlogging and submergence. Ann Rev of Plant Physiol 36(1):145–174
Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42(D1):D1182–D1187. https://doi.org/10.1093/nar/gkt1016
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360. https://doi.org/10.1038/nmeth.3317
Klessig DF, Choi HW, Dempsey DA (2018) Systemic acquired resistance and salicylic acid: past, present, and future. Mol Plant Microbe Interact 31(9):871–888. https://doi.org/10.1094/MPMI-03-18-0067-CR
Kong Q, Yuan J, Niu P, Xie J, Jiang W, Huang Y, Bie Z (2014) Screening suitable reference genes for normalization in reverse transcription quantitative real-time pcr analysis in melon. PLoS ONE 9(1):e87197. https://doi.org/10.1371/journal.pone.0087197
Kumutha D, Sairam RK, Ezhilmathi K, Chinnusamy V, Meena RC (2008) Effect of waterlogging on carbohydrate metabolism in pigeon pea (Cajanus cajan L.): upregulation of sucrose synthase and alcohol dehydrogenase. Plant Sci 175(5):706–716. https://doi.org/10.1016/j.plantsci.2008.07.013
Landrein B, Hamant O (2013) How mechanical stress controls microtubule behavior and morphogenesis in plants: history, experiments and revisited theories. Plant J 75(2):324–338. https://doi.org/10.1111/tpj.12188
Li S-W, Xue L, Xu S, Feng H, An L (2009) Mediators, genes and signaling in adventitious rooting. Bot Rev 75(2):230–247. https://doi.org/10.1007/s12229-009-9029-9
Licausi F, van Dongen JT, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P (2010) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J 62(2):302–315. https://doi.org/10.1111/j.1365-313X.2010.04149.x
Lin KHR, Weng CC, Lo HF, Chen JT (2004) Study of the root antioxidative system of tomatoes and eggplants under waterlogged conditions. Plant Sci 167(2):355–365. https://doi.org/10.1016/j.plantsci.2004.04.004
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8
Ma B, Yin CC, He SJ, Lu X, Zhang WK, Lu TG, Chen SY, Zhang JS (2014) Ethylene-induced inhibition of root growth requires abscisic acid function in rice (Oryza sativa L.) seedlings. PLoS Genet. https://doi.org/10.1371/journal.pgen.1004701
Mergemann H, Sauter M (2000) Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol 124(2):609–614. https://doi.org/10.1104/pp.124.2.609
Minami A, Yano K, Gamuyao R, Nagai K, Kuroha T, Ayano M, Nakamori M, Koike M, Kondo Y, Niimi Y, Kuwata K, Suzuki T, Higashiyama T, Takebayashi Y, Kojima M, Sakakibara H, Toyoda A, Fujiyama A, Kurata N, Ashikari M, Reuscher S (2018) Time-course transcriptomics analysis reveals key responses of submerged deepwater rice to flooding. Plant Physiol 176(4):3081–3102. https://doi.org/10.1104/pp.17.00858
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(10):490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Narsai R, Rocha M, Geigenberger P, Whelan J, van Dongen JT (2011) Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol 190(2):472–487. https://doi.org/10.1111/j.1469-8137.2010.03589.x
Nuñez-Palenius HG, Gomez-Lim M, Ochoa-Alejo N, Grumet R, Lester G, Cantliffe DJ (2008) Melon fruits: genetic diversity, physiology, and biotechnology features. Crit Rev Biotechnol 28(1):13–55. https://doi.org/10.1080/07388550801891111
Pacurar DI, Perrone I, Bellini C (2014) Auxin is a central player in the hormone cross-talks that control adventitious rooting. Physiol Plantarum 151(1):83–96. https://doi.org/10.1111/ppl.12171
Pang J, Cuin T, Shabala L, Zhou M, Mendham N, Shabala S (2007) Effect of secondary metabolites associated with anaerobic soil conditions on ion fluxes and electrophysiology in barley roots. Plant Physiol 145(1):266–276. https://doi.org/10.1104/pp.107.102624
Papdi C, Pérez-Salamó I, Joseph MP, Giuntoli B, Bögre L, Koncz C, Szabados L (2015) The low oxygen, oxidative and osmotic stress responses synergistically act through the ethylene response factor VII genes RAP2.12, RAP2.2 and RAP2.3. Plant J 82(5):772–784. https://doi.org/10.1111/tpj.12848
Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33(3):290–295. https://doi.org/10.1038/nbt.3122
Ren CG, Kong CC, Yan K, Zhang H, Luo YM, Xie ZH (2017) Elucidation of the molecular responses to waterlogging in Sesbania cannabina roots by transcriptome profiling. Sci Rep 7:9256. https://doi.org/10.1038/s41598-017-07740-5
Ricard B, Toai TV, Chourey P, Saglio P (1998) Evidence for the critical role of sucrose synthase for anoxic tolerance of maize roots using a double mutant. Plant Physiol 116(4):1323–1331. https://doi.org/10.1104/pp.116.4.1323
Rigal A, Yordanov YS, Perrone I, Karlberg A, Tisserant E, Bellini C, Busov VB, Martin F, Kohler A, Bhalerao R, Legué V (2012) The AINTEGUMENTA LIKE1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia in poplar. Plant Physiol 160(4):1996–2006. https://doi.org/10.1104/pp.112.204453
Ruan J, Zhou Y, Zhou M, Yan J, Khurshid M, Weng W, Cheng J, Zhang K (2019) Jasmonic acid signaling pathway in plants. Int J Mol Sci 20:2479. https://doi.org/10.3390/ijms20102479
Sasidharan R, Voesenek LACJ (2015) Ethylene-mediated acclimations to flooding stress. Plant Physiol 169(1):3–12. https://doi.org/10.1104/pp.15.00387
Schnittger A, Schobinger U, Stierhof YD, Hulskamp M (2002) Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr Biol 12(5):415–420. https://doi.org/10.1016/s0960-9822(02)00693-0
Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant Soil 253(1):1–34
Shabala S (2011) Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. New Phytol 190(2):289–298. https://doi.org/10.1111/j.1469-8137.2010.03575.x
Shimamura S, Yoshida S, Mochizuki T (2007) Cortical aerenchyma formation in hypocotyl and adventitious roots of luffa cylindrica subjected to soil flooding. Ann Bot 100(7):1431–1439. https://doi.org/10.1093/aob/mcm239
Shiono K, Takahashi H, Colmer TD, Nakazono M (2008) Role of ethylene in acclimations to promote oxygen transport in roots of plants in waterlogged soils. Plant Sci 175(1–2):52–58. https://doi.org/10.1016/j.plantsci.2008.03.002
Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170(2):603–617. https://doi.org/10.1104/pp.15.01360
Steffens B, Sauter M (2009) Epidermal cell death in rice is confined to cells with a distinct molecular identity and is mediated by ethylene and H2O2 through an autoamplified signal pathway. Plant Cell 21(1):184–196. https://doi.org/10.1105/tpc.108.061887
Steffens B, Wang J, Sauter M (2006) Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223(3):604–612. https://doi.org/10.1007/s00425-005-0111-1
Valliyodan B, Van Toai T, Alves J, de Fátima P, Goulart P, Lee J, Fritschi F, Rahman M, Islam R, Shannon J, Nguyen H (2014) Expression Of Root-Related Transcription Factors Associated With Flooding Tolerance Of Soybean (Glycine max). Int J Mol Sci 15(10):17622–17643. https://doi.org/10.3390/ijms151017622
Verstraeten I, Sb S, Geelen D (2014) Hypocotyl adventitious root organogenesis differs from lateral root development. Front Plant Sci 5:495. https://doi.org/10.3389/fpls.2014.00495
Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63(4):551–562. https://doi.org/10.1111/j.1365-313X.2010.04262.x
Visser E, Cohen JD, Barendse G, Blom C, Voesenek L (1996) An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustris Sm. Plant Physiol 112(4):1687–1692. https://doi.org/10.1104/pp.112.4.1687
Voesenek L, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytol 206(1):57–73. https://doi.org/10.1111/nph.13209
Voesenek LACJ, Sasidharan R, Weber A (2013) Ethylene-and oxygen signaling—drive plant survival during flooding. Plant Biol 15(3):426–435. https://doi.org/10.1111/plb.12014
Wample RL, Reid DM (1975) Effect of aeration on the flood-induced formation of adventitious roots and other changes in sunflower (Helianthus annuus L.). Planta 127(3):263–270. https://doi.org/10.1007/BF00380723
Wang H, Sui X, Guo J, Wang Z, Cheng J, Ma SI, Li X, Zhang Z (2014) Antisense suppression of cucumber (Cucumis sativus L.) sucrose synthase 3 (CsSUS3) reduces hypoxic stress tolerance. Plant Cell Environ 37(3):795–810. https://doi.org/10.1111/pce.12200
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C-Y, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. https://doi.org/10.1093/nar/gkr483
Xu X, Chen M, Ji J, Xu Q, Qi X, Chen X (2017) Comparative RNA-seq based transcriptome profiling of waterlogging response in cucumber hypocotyls reveals novel insights into the de novo adventitious root primordia initiation. BMC Plant Biol 17:129. https://doi.org/10.1186/s12870-017-1081-8
Xu X, Ji J, Xu Q, Qi X, Weng Y, Chen X (2018) The major-effect quantitative trait locus CsARN6.1 encodes an AAA ATPase domain-containing protein that is associated with waterlogging stress tolerance by promoting adventitious root formation. Plant J 93(5):917–930. https://doi.org/10.1111/tpj.13819
Yang R, Yang T, Zhang H, Qi Y, Xing Y, Zhang N, Li R, Weeda S, Ren S, Ouyang B, Guo Y-D (2014) Hormone profiling and transcription analysis reveal a major role of ABA in tomato salt tolerance. Plant Physiol Bioch 77:23–34. https://doi.org/10.1016/j.plaphy.2014.01.015
Zhang H, Cao N, Dong C, Shang Q (2017) Genome-wide identification and expression of arf gene family during adventitious root development in hot pepper (Capsicum annuum ). Hortic Plant J 3(4):151–164. https://doi.org/10.1016/j.hpj.2017.07.001
Zhang H, Cao N, Yang H, Li G, Zhu F (2019) Cloning and expression analysis of CmCRL1 in melon. Acta Hortic Sin 46(10):1989–1998. https://doi.org/10.16420/j.issn.0513-353x.2019-0004
Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5(2):334–338. https://doi.org/10.1093/mp/ssr104
Zhu X, Li X, Jiu S, Zhang K, Wang C, Fang J (2018) Analysis of the regulation networks in grapevine reveals response to waterlogging stress and candidate gene-marker selection for damage severity. Roy Soc Open Sci 5(6):172253. https://doi.org/10.1098/rsos.172253
Acknowledgements
This work was supported by the Jiangxi Province Science Foundation for Youths (20192BAB214017), the Modern Agricultural Research Collaborative Innovation Program of Jiangxi Province (JXXTCXQN202007), the Innovation Program of Jiangxi Academy of Agricultural Sciences (20181CBS002), the China Agriculture Research System (CARS-25), the Modern Agricultural Research Collaborative Innovation Program of Jiangxi Province (JXXTCX202109), the Special Fund for Agro-scientific Research in the Public Interest (201503110-05), and the Science and Technology Support Program of Jiangxi Province (20151BBF60053).
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FZ and ML designed the experiments. HZ conducted experiments and data analysis, and wrote the manuscript. GL conducted data analysis. CY, NC and HY revised the manuscript. All authors read and approved the manuscript.
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Supplementary file1 Suppl Table 1 The primer sequences for qRT-PCR. Suppl Table 2 The Pearson coefficient of samples. Suppl Table 3 An overview of gene expression level. Suppl Table 4 The detailed information of differentially expressed genes. Suppl Table 5 GO enrichment analysis of the four trend profiles in DEGs. Suppl Table 6 KEGG enrichment analysis of four trend profiles in DEGs. Suppl Table 7 KEGG enrichment analysis of the commonly up-regulated and down-regulated DEGs. Suppl Table 8 The DEGs associated with reactive oxygen species scavenging. Suppl Table 9 The DEGs of cellular activity-related genes. Suppl Table 10 The DEGs associated with hormone metabolism. Suppl Table 11 List of differentially expressed genes annotated as transcription factors. Suppl Table 12 Genes with GCC box in the promoter region. Suppl Table 13 The 251 DEGs with GCC box in the promoter region. Suppl Table 14 GO enrichment analysis of the 251 DEGs with GCC box in the promoter region. (DOCX 993 KB)
13205_2021_2866_MOESM2_ESM.xlsx
Supplementary file2 Suppl Fig. 1 GO enrichment of the genes commonly expressed in all samples. BP, biological processes; MF, molecular function; CC, cellular component. Suppl Fig. 2 The comparison of RNA-seq data and corresponding qRT-PCR data at different time intervals. The black line shows the results of RNA-seq, and the gray histogram shows the results of qRT-PCR. The CmACT gene was used as the internal control for qRT-PCR. ACC synthase, 1-aminocyclopropane-1-carboxylate synthase; ACC oxidase, 1-aminocyclopropane-1-carboxylate oxidase; NCED, 9-cis-epoxycarotenoid dioxygenase. (XLSX 1341 KB)
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Zhang, H., Li, G., Yan, C. et al. Depicting the molecular responses of adventitious rooting to waterlogging in melon hypocotyls by transcriptome profiling. 3 Biotech 11, 351 (2021). https://doi.org/10.1007/s13205-021-02866-w
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DOI: https://doi.org/10.1007/s13205-021-02866-w