Effects of waterlogging stress on early seedling development and transcriptomic responses in Brassica napus

Abstract

In this study, we performed a transcriptomic analysis to investigate genome-wide gene profiles of a rapeseed (Brassica napus) cultivar Zhongshuang 11 (ZS11) in response to waterlogging stress at germination stage. The root and shoot development of ZS11 was dramatically inhibited by waterlogging stress. As a result, 7472 downregulated DEGs (differentially expressed genes) and 3869 upregulated DEGs were identified by the RNA-seq experiments. KEGG analyses show that enriched pathways of these DEGs mainly include “plant hormone signal transduction,” “phenylpropanoid biosynthesis,” and “starch and sucrose metabolism.” Among them, there are 41, 19, and 26 DEGs involved in the regulatory pathways of root, shoot, and hypocotyl growth, respectively. In detail, the downregulated IAA17, IAA28, YUCCA9, UPBEAT1, and ARR1 and the upregulated ACR4 probably affect the balance between cell differentiation and division in the root apical meristem (RAM), while the downregulated CLV1, CRN, AHK4, and FAS2 might disturb stem cell fate in the shoot apical meristem (SAM). Taken together, the current results provide valuable information for understanding molecular mechanisms of seedling development in response to waterlogging stress at germination stage in rapeseed.

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References

  1. Bai M, Fan M, Oh E, Wang Z (2012) A triple helix-loop-helix/basic helix-loop-helix cascade controls cell elongation downstream of multiple hormonal and environmental signaling pathways in Arabidopsis. Plant Cell 24(12):4917–4929. https://doi.org/10.1105/tpc.112.105163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LACJ, Van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17(3):129–138. https://doi.org/10.1016/j.tplants.2011.12.004

    Article  PubMed  CAS  Google Scholar 

  3. Bäurle I, Laux T (2003) Apical meristems: the plant’s fountain of youth. Bioessays 25(10):961–970. https://doi.org/10.1002/bies.10341

    Article  CAS  Google Scholar 

  4. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289(5479):617–619. https://doi.org/10.1126/science.289.5479.617

    Article  PubMed  CAS  Google Scholar 

  5. Carles CC, Fletcher JC (2003) Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci 8(8):394–401. https://doi.org/10.1016/s1360-1385(03)00164-x

    Article  PubMed  CAS  Google Scholar 

  6. Causier B, Ashworth M, Guo WJ, Davies B (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158(1):423–438. https://doi.org/10.1104/pp.111.186999

    Article  PubMed  CAS  Google Scholar 

  7. Cazzonelli CI, Vanstraelen M, Simon S, Yin KD, Carron-Arthur A, Nisar N, Tarle G, Cuttriss AJ, Searle IR, Benkova E, Mathesius U, Masle J, Friml J, Pogson BJ (2013) Role of the Arabidopsis PIN6 auxin transporter in auxin homeostasis and auxin-mediated development. PLoS One 8(7):e700697. https://doi.org/10.1371/journal.pone.0070069

    Article  CAS  Google Scholar 

  8. Chen CJ, Xia R, Chen H, He YH (2018) TBtools, a toolkit for biologists integrating various HTS-data handling tools with a user-friendly interface. bioRxiv:289660. https://doi.org/10.1101/289660

  9. Cheng Y, Gu M, Cong Y, Zou CS, Zhang XK, Wang HZ (2010) Combining ability and genetic effects of germination traits of Brassica napus L. under waterlogging stress condition. Agric Sci China 9(7):951–957. https://doi.org/10.1016/S1671-2927(09)60176-0

    Article  Google Scholar 

  10. Cheng S, Huang Y, Zhu N, Zhao Y (2014) The rice WUSCHEL-related homeobox genes are involved in reproductive organ development, hormone signaling and abiotic stress response. Gene 549(2):266–274. https://doi.org/10.1016/j.gene.2014.08.003

    Article  PubMed  CAS  Google Scholar 

  11. Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signalling during plant flooding. Plant Physiol Biochem 42(4):273–282. https://doi.org/10.1016/j.plaphy.2004.02.003

    Article  PubMed  CAS  Google Scholar 

  12. De Lucas M, Daviere JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451(7177):480–484. https://doi.org/10.1038/nature06520

    Article  CAS  Google Scholar 

  13. De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S, Möller B, Wilson M, Holman T, Van Isterdael G, Brunoud G, Vuylsteke M, Vernoux T, De Veylder L, Inzé D, Weijers D, Bennett MJ, Beeckman T (2010) A novel Aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr Biol 20(19):1697–1706. https://doi.org/10.1016/j.cub.2010.09.007

    Article  PubMed  CAS  Google Scholar 

  14. Ding ZJ, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci U S A 107(26):12046–12051. https://doi.org/10.1073/pnas.1000672107

    Article  PubMed  PubMed Central  Google Scholar 

  15. Dossa K, You J, Wang LH, Zhang YX, Li DH, Zhou R, Yu JY, Wei X, Zhu XD, Jiang SY, Gao Y, Mmadi MA, Zhang XR (2019) Transcriptomic profiling of sesame during waterlogging and recovery. Sci Data 6(1):1–5. https://doi.org/10.1038/s41597-019-0226-z

    Article  CAS  Google Scholar 

  16. Gaillochet C, Daum G, Lohmann JU (2015) O cell, where art thou? The mechanisms of shoot meristem patterning. Curr Opin Plant Biol 23:91–97. https://doi.org/10.1016/j.pbi.2014.11.002

    Article  PubMed  Google Scholar 

  17. Gibbs DJ, Lee SC, Isa NM, Gramuglia S, Fukao T, Bassel GW, Correia CS, Corbineau F, Theodoulou FL, Bailey-Serres J, Holdsworth MJ (2011) Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature 479(7373):415–418. https://doi.org/10.1038/nature10534

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci U S A 106(38):16529–16534. https://doi.org/10.1073/pnas.0908122106

    Article  PubMed  PubMed Central  Google Scholar 

  19. Hao YQ, Oh E, Choi G, Liang ZS, Wang ZY (2012) Interactions between HLH and bHLH factors modulate light-regulated plant development. Mol Plant 5(3):688–697. https://doi.org/10.1093/mp/sss011

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. 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. https://doi.org/10.1104/pp.110.155077

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29(5):649–659. https://doi.org/10.1046/j.0960-7412.2001.01247.x

    Article  CAS  Google Scholar 

  22. Jackson MB, Colmer TD (2005) Response and adaptation by plants to flooding stress. Ann Bot (Oxford, U. K.) 96(4):501–505. https://doi.org/10.1093/aob/mci205

    Article  CAS  Google Scholar 

  23. Jaiswal A, Srivastava JP (2018) Changes in reactive oxygen scavenging systems and protein profiles in maize roots in response to nitric oxide under waterlogging stress. Indian J Biochem Biophys 55(1):26–33

    CAS  Google Scholar 

  24. Jia KP, Luo Q, He SB, Lu XD, Yang HQ (2014) Strigolactone-regulated hypocotyl elongation is dependent on cryptochrome and phytochrome signaling pathways in Arabidopsis. Mol Plant 7(3):528–540. https://doi.org/10.1093/mp/sst093

    Article  PubMed  CAS  Google Scholar 

  25. Kamiya Y, Garcı́a-Martı́nez JL (1999) Regulation of gibberellin biosynthesis by light. Curr Opin Plant Biol 2(5):398–403. https://doi.org/10.1016/s1369-5266(99)00012-6

    Article  PubMed  CAS  Google Scholar 

  26. Kaya H, Shibahara K, Taoka K, Iwabuchi M, Stillman B, Araki T (2001) FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104(1):131–142. https://doi.org/10.1016/s0092-8674(01)00197-0

    Article  PubMed  CAS  Google Scholar 

  27. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2012) TopHat2: parallel mapping of transcriptomes to detect InDels, gene fusions, and more. Genomics Inf 10:263–265. https://doi.org/10.1186/gb-2013-14-4-r36

    Article  CAS  Google Scholar 

  28. Kitagawa M, Jackson D (2019) Control of meristem size. Annu Rev Plant Biol 70:269–291. https://doi.org/10.1146/annurev-arplant-042817-040549

    Article  PubMed  CAS  Google Scholar 

  29. Laux T, Mayer KFX, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122(1):87–96

    PubMed  CAS  Google Scholar 

  30. Li J, Terzaghi W, Gong YY, Li CR, Ling JJ, Fan YY, Qin NX, Gong XQ, Zhu DM, Deng XW (2020) Modulation of BIN2 kinase activity by HY5 controls hypocotyl elongation in the light. Nat Commun 11(1):15921. https://doi.org/10.1038/s41467-020-15394-7

    Article  CAS  Google Scholar 

  31. 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

    Article  PubMed  CAS  Google Scholar 

  32. Liu FL, VanToai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137(3):1115–1129. https://doi.org/10.1104/pp.104.055475

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Liu PQ, Sun F, Gao R, Dong HS (2012) RAP2. 6L overexpression delays waterlogging induced premature senescence by increasing stomatal closure more than antioxidant enzyme activity. Plant Mol Biol 79(6):609–622. https://doi.org/10.1007/s11103-012-9936-8

    Article  PubMed  CAS  Google Scholar 

  34. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Loreti E, van Veen H, Perata P (2016) Plant responses to flooding stress. Curr Opin Plant Biol 33:64–71. https://doi.org/10.1016/j.pbi.2016.06.005

    Article  PubMed  CAS  Google Scholar 

  36. Mendiondo GM, Gibbs DJ, Szurman-Zubrzycka M, Korn A, Marquez J, Szarejko I, Maluszynski M, King J, Axcell B, Smart K, Corbineau F, Holdsworth MJ (2016) Enhanced waterlogging tolerance in barley by manipulation of expression of the N-end rule pathway E3 ligase PROTEOLYSIS 6. Plant Biotechnol J 14(1):40–50. https://doi.org/10.1111/pbi.12334

    Article  PubMed  CAS  Google Scholar 

  37. Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14(7):399–408. https://doi.org/10.1016/j.tplants.2009.05.002

    Article  PubMed  CAS  Google Scholar 

  38. Pertea M, Pertea GM, Antonescu CM, Chang TC, 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590. https://doi.org/10.1146/annurev-arplant-042811-105501

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Ponnu J, Riedel T, Penner E, Schrader A, Hoecker U (2019) Cryptochrome 2 competes with COP1 substrates to repress COP1 ubiquitin ligase activity during Arabidopsis photomorphogenesis. Proc Natl Acad Sci U S A 116(52):27133–27141. https://doi.org/10.1073/pnas.1909181116

    Article  PubMed Central  CAS  Google Scholar 

  41. Quail PH (1994) Photosensory perception and signal-transduction in plants. Curr Opin Genet Dev 4(5):652–661. https://doi.org/10.1016/0959-437x(94)90131-l

    Article  PubMed  CAS  Google Scholar 

  42. Ren H, Gray WM (2015) SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant 8(8):1153–1164. https://doi.org/10.1016/j.molp.2015.05.003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Ruperti B, Botton A, Populin F, Eccher G, Brilli M, Quaggiotti S, Trevisan S, Cainelli N, Guarracino P, Schievano E (2019) Flooding responses on grapevine: a physiological, transcriptional, and metabolic perspective. Front Plant Sci 10(339). https://doi.org/10.3389/fpls.2019.00339

  44. Sacks MM, Silk WK, Burman P (1997) Effect of water stress on cortical cell division rates within the apical meristem of primary roots of maize. Plant Physiol 114(2):519–527. https://doi.org/10.1104/pp.114.2.519

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22(11):3560–3573. https://doi.org/10.1105/tpc.110.074641

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Sparks EE, Benfey PN (2014) HEC of a job regulating stem cells. Dev Cell 28(4):349–350. https://doi.org/10.1016/j.devcel.2014.02.006

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19(11):909–914. https://doi.org/10.1016/j.cub.2009.03.060

    Article  PubMed  CAS  Google Scholar 

  48. Sun LR, Ma LY, He SB, Hao FS (2018) AtrbohD functions downstream of ROP2 and positively regulates waterlogging response in Arabidopsis. Plant Signal Behav 13:e1513300. https://doi.org/10.1080/15592324.2018.1513300

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Tanimoto E (2005) Regulation of root growth by plant hormones-Roles for auxin and gibberellin. Crit Rev Plant Sci 24(4):249–265. https://doi.org/10.1080/07352680500196108

  50. Ugartechea-Chirino Y, Swarup R, Swarup K, Peret B, Whitworth M, Bennett M, Bougourd S (2010) The AUX1 LAX family of auxin influx carriers is required for the establishment of embryonic root cell organization in Arabidopsis thaliana. Ann Bot (Oxford, U. K.) 105(2):277–289. https://doi.org/10.1093/aob/mcp287

    Article  CAS  Google Scholar 

  51. Van Veen H, Vashisht D, Akman M, Girke T, Mustroph A, Reinen E, Hartman S, Kooiker M, Van Tienderen P, Schranz ME, Bailey-Serres J, Voesenek LACJ, Sasidharan R (2016) Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype-and organ-specific responses to flooding stress. Plant Physiol 172(2):668–689. https://doi.org/10.1104/pp.16.00472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63. https://doi.org/10.1038/nrg2484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Wang PF, Wang YM, Ren FS (2019) Genome-wide identification of the CLAVATA3/EMBRYO SURROUNDING REGION (CLE) family in grape (Vitis vinifera L.). BMC Genomics 20(553):553. https://doi.org/10.1186/s12864-019-5944-2

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Williams L, Fletcher JC (2005) Stem cell regulation in the Arabidopsis shoot apical meristem. Curr Opin Plant Biol 8(6):582–586. https://doi.org/10.1016/j.pbi.2005.09.010

    Article  PubMed  CAS  Google Scholar 

  55. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442(7103):705–708. https://doi.org/10.1038/nature04920

    Article  PubMed  CAS  Google Scholar 

  56. Xu MY, Ma HQ, Zeng L, Cheng Y, Lu GY, Xu JS, Zhang XK, Zou XL (2015) The effect of waterlogging on yield and seed quality at the early flowering stage in Brassica napus L. Field Crop Res 180:238–245. https://doi.org/10.1016/j.fcr.2015.06.007

    Article  Google Scholar 

  57. Xu BB, Cheng Y, Zou XL, Zhang XK (2016) Ethanol content in plants of Brassica napus L. correlated with waterlogging tolerance index and regulated by lactate dehydrogenase and citrate synthase. Acta Physiol Plant 38(3):81. https://doi.org/10.1007/s11738-016-2098-6

    Article  CAS  Google Scholar 

  58. Yang ZE, Gong Q, Qin WQ, Yang ZR, Cheng Y, Lu LL, Ge XY, Zhang CJ, Wu ZX, Li FG (2017) Genome-wide analysis of WOX genes in upland cotton and their expression pattern under different stresses. BMC Plant Biol 17:113. https://doi.org/10.1186/s12870-017-1065-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Zaman MSU, Malik AI, Erskine W, Kaur P (2019) Changes in gene expression during germination reveal pea genotypes with either “quiescence” or “escape” mechanisms of waterlogging tolerance. Plant Cell Environ 42(1):245–258. https://doi.org/10.1111/pce.13338

    Article  PubMed  CAS  Google Scholar 

  60. Zhang XC, Fan Y, Shabala S, Koutoulis A, Shabala L, Johnson P, Hu HL, Zhou MX (2017) A new major-effect QTL for waterlogging tolerance in wild barley (H. spontaneum). Theor Appl Genet 130(8):1559–1568. https://doi.org/10.1007/s00122-017-2910-8

    Article  PubMed  CAS  Google Scholar 

  61. Zhang YP, Ou LJ, Zhao J, Liu ZB, Li XF (2019) Transcriptome analysis of hot pepper plants identifies waterlogging resistance related genes. Chil J Agric Res 79(2):296–306. https://doi.org/10.4067/S0718-58392019000200296

    Article  Google Scholar 

  62. Zhu DM, Maier A, Lee JH, Laubinger S, Saijo Y, Wang H, Qu LJ, Hoecker U, Deng XW (2008) Biochemical characterization of Arabidopsis complexes containing CONSTITUTIVELY PHOTOMORPHOGENIC1 and SUPPRESSOR OF PHYA proteins in light control of plant development. Plant Cell 20(9):2307–2323. https://doi.org/10.1105/tpc.107.056580

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Zou XL, Zeng L, Lu GY, Cheng Y, Xu JS, Zhang XK (2015) Comparison of transcriptomes undergoing waterlogging at the seedling stage between tolerant and sensitive varieties of Brassica napus L. J Integr Agric 14(9):1723–1734. https://doi.org/10.1016/s2095-3119(15)61138-8

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Dr. J.M. Xu (Zhejiang University, China) for the technical support.

Funding

This research was supported by Jiangsu Collaborative Innovation Center for Modern Crop Production.

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YY Guo and DZ Wu designed the research. YY Guo, J Chen, NH Wang, LH Kuang, LX Jiang, GP Zhang, and DZ Wu performed the research. YY Guo and DZ Wu analyzed the data. YY Guo and DZ Wu wrote the article. The authors declare no conflict of interest.

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Correspondence to Dezhi Wu.

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Guo, Y., Chen, J., Kuang, L. et al. Effects of waterlogging stress on early seedling development and transcriptomic responses in Brassica napus. Mol Breeding 40, 85 (2020). https://doi.org/10.1007/s11032-020-01167-z

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Keywords

  • Brassica napus
  • Waterlogging tolerance
  • Transcriptomics
  • Root apical meristem
  • Shoot apical meristem