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Integrative transcriptomic and metabolomic analyses provide insight into the long-term submergence response mechanisms of young Salix variegata stems

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Abstract

Main conclusion

The mechanisms underlying long-term complete submergence tolerance in S. variegata involve enhanced oxidative stress responses, strengthened ethylene and ABA signaling, synthesis of raffinose family oligosaccharides, unsaturated fatty acids, and specific stress-related amino acids.

Abstract

Salix variegata Franch. is a riparian shrub species that can tolerate long-term complete submergence; however, the molecular mechanisms underlying this trait remain to be elucidated. In this study, we subjected S. variegata plants to complete submergence for 60 d and collected stems to perform transcriptomic and metabolomic analyses, as well as quantitative reverse transcription-polymerase chain reaction (qRT-PCR) assays. Results revealed that photosynthesis and the response to light stimulus were inhibited during submergence and recovered after desubmergence. Ethylene and abscisic acid (ABA) signaling could be important for the long-term submergence tolerance of S. variegata. Jasmonic acid (JA) signaling also participated in the response to submergence. Raffinose family oligosaccharides, highly unsaturated fatty acids, and specific stress-related amino acids accumulated in response to submergence, indicating that they may protect plants from submergence damage, as they do in response to other abiotic stressors. Several organic acids were produced in S. variegata plants after submergence, which may facilitate coping with the toxicity induced by submergence. After long-term submergence, cell wall reorganization and phenylpropanoid metabolic processes (the synthesis of specific phenolics and flavonoids) were activated, which may contribute to long-term S. variegata submergence tolerance; however, the detailed mechanisms require further investigation. Several transcription factors (TFs), such as MYB, continuously responded to submergence, indicating that they may play important roles in the responses and adaption to submergence. Genes related to oxidative stress tolerance were specifically expressed after desubmergence, potentially contributing to recovery of S. variegata plants within a short period of time.

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Abbreviations

DEGs:

Differentially expressed genes

ERF:

Ethylene response factor

JA:

Jasmonic acid

TGRR:

Three Gorges Reservoir region

TF:

Transcription factor

References

  • Alpuerto JB, Hussain RMF, Fukao T (2016) The key regulator of submergence tolerance, SUB1A, promotes photosynthetic and metabolic recovery from submergence damage in rice leaves. Plant Cell Environ 39:672–684

    Article  CAS  PubMed  Google Scholar 

  • Ayano M, Kani T, Kojima M, Sakakibara H, Ashikari M (2014) Gibberellin biosynthesis and signal transduction is essential for internode elongation in deepwater rice. Plant Cell Environ 37:2313–2324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey-Serres J, Voesenek L (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339

    Article  CAS  PubMed  Google Scholar 

  • Benschop JJ, Jackson MB, Gühl K, Vreeburg RAM, Voesenek LACJ (2006) Contrasting interactions between ethylene and abscisic acid in Rumex species differing in submergence tolerance. Plant J 44:756–768

    Article  CAS  Google Scholar 

  • Chen ZC, Liao H (2016) Organic acid anions: An effective defensive weapon for plants against aluminum toxicity and phosphorus deficiency in acidic soils. J Genet Genomics 43:631–638

    Article  PubMed  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • ElSayed A, Rafudeen M, Golldack D (2014) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol 16:1–8

    Article  CAS  PubMed  Google Scholar 

  • Fukao T, Yeung E, Bailey-Serres J (2012) The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness through hormonal regulation in rice. Plant Physiol 160:1795–1807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukao T, Barrera-Figueroa BE, Juntawong P, Peña-Castro JM (2019) Submergence and waterlogging stress in plants: a review highlighting research opportunities and understudied aspects. Front Plant Sci 10:340

    Article  PubMed  PubMed Central  Google Scholar 

  • Gibbs DJ, Lee SC, Isa NM, Gramuglia S, Fukao T, Bassel GW, Correia CS, Fo C, Theodoulou FL, Bailey-Serres J (2011) Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature 479:415–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gustafsson H (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39:969–987

    Article  CAS  Google Scholar 

  • Karrenberg S, Edwards PJ, Kollmann J (2002) The life history of Salicaceae living in the active zone of floodplains. Freshwater Biol 47:733–748

    Article  Google Scholar 

  • Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229

    Article  CAS  PubMed  Google Scholar 

  • Kreuzwieser J, Rennenberg H (2014) Molecular and physiological responses of trees to waterlogging stress. Plant Cell Environ 37:2245–2259

    CAS  PubMed  Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8’-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SC, Mustroph A, Sasidharan R, Vashisht D, Pedersen O, Oosumi T, Voesenek LACJ, Bailey-Serres J (2011) Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia. New Phytol 190:457–471

    Article  CAS  PubMed  Google Scholar 

  • Lei S, Zeng B, Xu S, Zhang X (2017) Response of basal metabolic rate to complete submergence of riparian species Salix variegata in the Three Gorges reservoir region. Sci Rep 7:13885

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li S, Pezeshki S, Goodwin S, Shields F (2004) Physiological responses of black willow (Salix nigra) cuttings to a range of soil moisture regimes. Photosynthetica 42:585–590

    Article  CAS  Google Scholar 

  • Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, Perata P, van Dongen JT (2011) Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479:419–422

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Ma D, Zhang Z, Wang S, Du S, Deng X, Yin L (2019) Plant lipid remodeling in response to abiotic stresses. Environ Exp Bot 165:174–184

    Article  CAS  Google Scholar 

  • Memon AR, Schröder P (2009) Implications of metal accumulation mechanisms to phytoremediation. Environ Sci Pollut R 16:162–175

    Article  CAS  Google Scholar 

  • Miao L, Xiao F, Xu W, Yang F (2016) Reconstruction of wetland zones: physiological and biochemical responses of Salix variegata to winter submergence: a case study from water level fluctuation zone of the Three Gorges Reservoir. Pol J Ecol 64:45–52

    Google Scholar 

  • Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27:64–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mustroph A, Lee SC, Oosumi T, Zanetti ME, Yang H, Ma K, Yaghoubi-Masihi A, Fukao T, Bailey-Serres J (2010) Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiol 152:1484–1500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 190:472–487

    Article  CAS  PubMed  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oh M-M, Trick HN, Rajashekar C (2009) Secondary metabolism and antioxidants are involved in environmental adaptation and stress tolerance in lettuce. J Plant Physiol 166:180–191

    Article  CAS  PubMed  Google Scholar 

  • Rivero RM, Ruiz JM, Garcıa PC, Lopez-Lefebre LR, Sánchez E, Romero L (2001) Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci 160:315–321

    Article  CAS  PubMed  Google Scholar 

  • Schreiber CM, Zeng B, Temperton VM, Rascher U, Kazda M, Schurr U, Höltkemeier A, Kuhn AJ (2011) Dynamics of organic acid occurrence under flooding stress in the rhizosphere of three plant species from the water fluctuation zone of the Three Gorges Reservoir, P.R. China Plant. Soil 344:111–129

    CAS  Google Scholar 

  • Sengupta S, Mukherjee S, Basak P, Majumder AL (2015) Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Front Plant Sci 6:656

    Article  PubMed  PubMed Central  Google Scholar 

  • Shingaki-Wells RN, Huang S, Taylor NL, Carroll AJ, Zhou W, Millar AH (2011) Differential molecular responses of rice and wheat coleoptiles to anoxia reveal novel metabolic adaptations in amino acid metabolism for tissue tolerance. Plant Physiol 156:1706–1724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su X, Zeng B, Lin F, Qiao P, Ayi Q, Huang W (2016) How does long-term complete submergence influence sex ratio and resource allocation of a dioecious shrub, Salix variegata Franch.? Ecol Eng 87:218–223

    Article  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 5:89–97

    Article  CAS  Google Scholar 

  • Tamang BG, Magliozzi JO, Maroof MAS, Fukao T (2014) Physiological and transcriptomic characterization of submergence and reoxygenation responses in soybean seedlings. Plant Cell Environ 37:2350–2365

    CAS  PubMed  Google Scholar 

  • Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30:967–977

    Article  CAS  PubMed  Google Scholar 

  • Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Voesenek LA, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytol 206:57–73

    Article  CAS  PubMed  Google Scholar 

  • Waters MT, Adrian S, Sun YK, Flematti GR, Smith SM (2015) The karrikin response system of Arabidopsis. Plant J 79:623–631

    Article  CAS  Google Scholar 

  • Yang F, Wang Y, Chan Z (2014) Perspectives on screening winter-flood-tolerant woody species in the riparian protection forests of the three Gorges Reservoir. PLoS ONE 9:e108725

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yeung E, Bailey-Serres J, Sasidharan R (2019) After the deluge: plant revival post-flooding. Trends Plant Sci 24:443–454

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Barg R, Yin M, Gueta-Dahan Y, Leikin-Frenkel A, Salts Y, Shabtai S, Ben-Hayyim G (2005) Modulated fatty acid desaturation via overexpression of two distinct ω-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. Plant J 44:361–371

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, Benner C, Chanda SK (2019) Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Comm 10:1523

    Article  CAS  Google Scholar 

  • Zhu J-K (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript. This research was supported by the Fundamental Research Funds for the Central Universities of China (Grant No. SWU118120), National Natural Science Foundation of China (31901283, 31870657 and 31800505), National Key Project for Research on Transgenic Plant (2016ZX08010-003), Natural Science Foundation Project of CQ CSTC (cstc2018jcyjAX0477), and Fundamental Research Funds for the Central Universities (XDJK2018AA005, XDJK2014a005).

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Authors and Affiliations

  1. Key Laboratory of Eco-Environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Tiansheng Road No. 2, Beibei, Chongqing, 400715, China

    Qingwei Zhang, Shaohu Tang, Jianqiu Li, Chunfen Fan & Keming Luo

  2. Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China

    Qingwei Zhang, Shaohu Tang, Jianqiu Li, Chunfen Fan & Keming Luo

  3. College of Horticulture, Northwest Agriculture and Forestry University, Yangling, 712100, Shaanxi, China

    Libo Xing

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  1. Qingwei Zhang
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Correspondence to Qingwei Zhang or Keming Luo.

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Supplementary Information

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425_2021_3604_MOESM1_ESM.xlsx

Supplementary Table S1 Statistical data of the transcriptomic analysis. Table S2 Statistical data of the transcripts mapped to the Salix genome. Table S3 Mapped transcript events in the Salix genome. Table S4 Number of transcripts that encoded proteins. Table S5 The number of DEGs at 0, 5, 10, 20, 40, and 60 d after submergence and 10 d after desubmergence. All groups were compared with the control (samples collected before the onset of submergence). Table S6 List of primer sequences used in the qRT-PCR assays. Table S7 Expression patterns of the homologous genes within the 49 core hypoxia-response genes. Table S8 List of upregulated transcription factor genes that were continuously expressed during submergence. Table S9 Detailed information regarding the genes presented in Figs. 8–12 and S2. (XLSX 34 KB)

425_2021_3604_MOESM2_ESM.xls

Supplementary Table S10 Gene expression profiles that changed 5 d after submergence compared to the control. Table S11 Gene expression profiles that changed 10 d after submergence compared to the control. Table S12 Gene expression profiles that changed 20 d after submergence compared to the control. Table S13 Gene expression profiles that changed 40 d after submergence compared to the control. Table S14 Gene expression profiles that changed 60 d after submergence compared to the control. Table S15 Gene expression profiles that changed 10 d after desubmergence compared to the control. Table S16 Gene expression profiles that changed after 60 d of normal growth compared to the control. Table S17 Gene expression profiles that changed 40 d after submergence compared to 60 d of normal growth. Table S18 Gene expression profiles that changed 60 d after submergence compared to 60 d of normal growth (XLS 86861 KB)

425_2021_3604_MOESM3_ESM.tif

Supplementary Fig. S1 The air temperature, water temperature, and water oxygen concentration data recorded during the experiment (TIF 152 KB)

425_2021_3604_MOESM4_ESM.tif

Supplementary Fig. S2 Gene expression profiles related to phenylpropanoid metabolic processes during submergence and after desubmergence. Note: C0 indicates the onset of submergence; S5, S10, S20, S40, and S60 indicate 5, 10, 20, 40, and 60 d after submergence, respectively; R10 indicates 10 d after desubmergence (TIF 126 KB)

425_2021_3604_MOESM5_ESM.tif

Supplementary Fig. S3 Results of the qRT-PCR assays of selected genes during submergence and the correlation analysis comparing the qRT-PCR and transcriptomic analysis results. Ubiquitin was used as the reference gene. All gene expression levels were normalized based on the reference gene’s expression levels. Note: C0 indicates the onset of submergence; S5, S10, S20, S40, and S60 indicate 5, 10, 20, 40, and 60 d after submergence, respectively; R10 indicates 10 d after desubmergence. The scatter plot was constructed using log2(qRT-PCR) as the independent variable and log2(FPKM) as the dependent variable (TIF 642 KB)

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Zhang, Q., Tang, S., Li, J. et al. Integrative transcriptomic and metabolomic analyses provide insight into the long-term submergence response mechanisms of young Salix variegata stems. Planta 253, 88 (2021). https://doi.org/10.1007/s00425-021-03604-5

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