Understanding physiological and molecular mechanisms of Populus deltoides ‘DanHongYang’ tolerance to waterlogging by comparative transcriptome analysis

Authors

  • Gang LI Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei; Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education (CN)
  • Qiusheng FU Hubei Ecology Polytechnic College, Department of Forestry Ecology, Wuhan 430070 (CN)
  • Zhongbin LIU Wuhan University of Bioengineering, School of Horticulture and Landscape, Wuhan 430415 (CN)
  • Jiabao YE Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Weiwei ZHANG Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Yongling LIAO Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei (CN)
  • Feng XU Yangtze University, College of Horticulture and Gardening, Jingzhou 434025, Hubei; Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education (CN)
  • Zhongcheng ZHOU Hubei Ecology Polytechnic College, Department of Forestry Ecology, Wuhan 430070 (CN)

DOI:

https://doi.org/10.15835/nbha48311977

Keywords:

antioxidant system; adventitious root; energy metabolism; Populus deltoides; transcriptome; transcription factor; waterlogging stress

Abstract

Populus deltoides ‘DanHongYang’ (DHY) was identified as a waterlogging-resistant cultivar in our previous study. Here, the phenotype, physiological features and transcriptome profiling of P. deltoides ‘DHY’ between the treatments of waterlogging and control were compared. Waterlogging treatment led to distinctly formation of adventitious roots from P. deltoides ‘DHY’ stems. The activities of ascorbate peroxidase and glutathione reductase significantly increased in the leaves of P. deltoides ‘DHY’ by waterlogging treatment. Comparative transcriptomic analysis showed that 2,447 and 9,465 differentially expressed genes (DEGs) were screened between the leaves and roots of P. deltoides ‘DHY’ under waterlogging and control, respectively. The KEGG analysis showed the most significantly up-regulated DEGs in the leaves and roots were enriched to the pathways of glycolyis and proline synthesis. Some genes involved in stress response, endogenous hormones, antioxidant system and adventitious root development in the waterlogged were identified to contribute to the waterlogging tolerance of P. deltoides ‘DHY’. In addition, some candidate transcription factors such as RAP, NAC, WRKY, and bHLH were also found to be associated with the waterlogging tolerance of P. deltoides ‘DHY’. These findings provided the insights into the physiological and molecular mechanisms underlying the tolerance of P. deltoides ‘DHY’ to waterlogging stresses.

References

Adamowski M, Friml J (2015). PIN-dependent auxin transport: action, regulation, and evolution. The Plant Cell 27(1):20-32. https://doi.org/10.1105/tpc.114.134874

Agulló-Antón MÁ, Ferrández-Ayela A, Fernández-García N, Nicolás C, Albacete A, Pérez-Alfocea F, … Acosta M (2014). Early steps of adventitious rooting: morphology, hormonal profiling and carbohydrate turnover in carnation stem cuttings. Physiologia Plantarum 150(3):446-462. https://doi.org/10.1111/ppl.12114

Ahmed S, Nawata E, Sakuratani T (2006). Changes of endogenous ABA and ACC, and their correlations to photosynthesis and water relations in mungbean (Vigna radiata (L.) Wilczak cv. KPS1) during waterlogging. Environmental and Experimental Botany 57(3):278-284. https://doi.org/10.1016/j.envexpbot.2005.06.006

Alia P, Sardhi P (1991). Proline accumulation under heavy metal stress. Journal of Plant Physiology 138(5):554-558.

Arbona V, Manzi M, Zandalinas SI, Vives-Peris V, Pérez-Clemente RM, Gómez-Cadenas A (2017).

Physiological, metabolic, and molecular responses of plants to abiotic stress. In: Stress Signaling in Plants: Genomics and Proteomics Perspective Volume 2 (Springer, Cham) pp 1-35. https://doi.org/10.1007/978-3-319-42183-4_1

Ariel FD, Diet A, Crespi M, Chan RL (2010). The LOB-like transcription factor MtLBD1 controls Medicago truncatula root architecture under salt stress. Plant Signaling & Behavior 5(12):1666-1668. https://doi.org/10.4161/psb.5.12.14020

Arora K, Panda KK, Mittal S, Mallikarjuna MG, Rao AR, Dash PK, Thirunavukkarasu N (2017). RNAseq revealed the important gene pathways controlling adaptive mechanisms under waterlogged stress in maize. Scientific Reporters 7(1):1-12. https://doi.org/10.1038/s41598-017-10561-1

Bailey-Serres J, Voesenek L (2008). Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59:313-339. https://doi.org/10.1146/annurev.arplant.59.032607.092752

Colmer TD (2003). Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell & Environment 26(1):17-36. https://doi.org/10.1046/j.1365-3040.2003.00846.x

Colmer TD, Voesenek LACJ (2009). Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36(8):665-681. https://doi.org/10.1071/fp09144

Coudert Y, Périn C, Courtois B, Khong NG, Gantet P (2010). Genetic control of root development in rice, the model cereal. Trends in Plant Science 15(4):219-226. https://doi.org/10.1016/j.tplants.2010.01.008

Dawood T, Yang X, Visser EJ, TeBeek TA, Kensche PR, Cristescu SM, Rieu I (2016). A co-opted hormonal cascade activates dormant adventitious root primordia upon waterlogging in Solanum dulcamara. Plant Physiology 170(4):2351-2364. https://doi.org/10.1104/pp.15.00773

De-Klerk GJ, Hanecakova J (2008). Ethylene and rooting of mung bean cuttings. The role of auxin induced ethylene synthesis and phase-dependent effects. Plant Growth Regulation 56(2):203. https://doi.org/10.1007/s10725-008-9301-8

DiDonato RJ, Arbuckle E, Buker S, Sheets J, Tobar J, Totong R, Celenza JL (2004). Arabidopsis ALF4 encodes a nuclear-localized protein required for lateral root formation. The Plant Journal 37(3):340-353. https://doi.org/10.1046/j.1365-313X.2003.01964.x

Doupis G, Kavroulakis N, Psarras G, Papadakis IE (2016). Growth, photosynthetic performance and antioxidative response of ‘Hass’ and ‘Fuerte’ avocado (Persea americana Mill.) plants grown under high soil moisture. Photosynthetica 55(4):655-663. https://doi.org/10.1007/s11099-016-0679-7

Du K, Xu L, Wu H, Tu B, Zheng B (2012). Ecophysiological and morphological adaption to soil flooding of two poplar clones differing in flood-tolerance Flora-Morphology, Distribution, Functional Ecology of Plants 207(2):96-106. https://doi.org/10.1016/j.flora.2011.11.002

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. Frontiers in Plant Science 10:340. https://doi.org/10.3389/fpls.2019.00340

Galmés J, Pou A, Alsina MM, Tomas M, Medrano H, Flexas J (2007). Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status. Planta 226(3):671-681. https://doi.org/10.2307/23389706

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I (2011). Full length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29(7):644. https://doi.org/10.1038/nbt.1883

He LZ, Li B, Lu XM, Yuan LY, Yang YJ, Yuan YH, Du J, Guo SR (2015). The effect of exogenous calcium on mitochondria, respiratory metabolism enzymes and ion transport in cucumber roots under hypoxia. Scientific Reports 5:11391. https://doi.org/10.1038/srep11391

Irfan M, Hayat S, Hayat Q, Afroz S, Ahmad A (2010). Physiological and biochemical changes in plants under waterlogging. Protoplasma 241:3-17. https://doi.org/ 10.1007/s00709-009-0098-8

Jackson MB, Ishizawa K, Ito O (2009). Evolution and mechanisms of plant tolerance to flooding stress. Annals of Botany 103:137-142. https://doi.org/10.1093/aob/mcn242

Jiang Y, Deyholos MK (2009). Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Molecular Biology 69(1-2):91-105. https://doi.org/10.1007/s11103-008-9408-3

Jing Z, Li, Z (2018). Genome-wide identification of wrky transcription factors in kiwifruit (Actinidia spp.) and analysis of wrky expression in responses to biotic and abiotic stresses. Genes & Genomics 40(4): 429-446. https://doi.org/.10.1007/s13258-017-0645-1

Kadam S, Abril A, Dhanapal AP, Koester RP, Vermerris W, Jose S, Fritschi FB (2017). Characterization and regulation of aquaporin genes of sorghum Sorghum bicolor (L.) Moench in response to waterlogging stress. Frontiers in Plant Science 8:862. https://doi.org/10.3389/fpls.2017.00862

Kim KN (2013). Stress responses mediated by the CBL calcium sensors in plants. Plant Biotechnology Reports 7(1):1-8. https://doi.org/0.1007/s11816-012-0228-1

Kim YH, Hwang SJ, Waqas M, Khan AL, Lee JH, Lee JD, Lee IJ (2015). Comparative analysis of endogenous hormones level in two soybeans (Glycine max L.) lines differing in waterlogging tolerance. Frontiers in Plant Science 6:714. https://doi.org/10.3389/fpls.2015.00714

Kramer EM, Ackelsberg EM (2015). Auxin metabolism rates and implications for plant development. Frontiers in Plant Science 6:150. https://doi.org/10.3389/fpls.2015.00150

Kravi N, Markovi K, Anelkovi V, Ukalovi HT, Babi V, Vuleti, M (2013). Growth, proline accumulation and peroxidase activity in maize seedlings under osmotic stress. Acta Physiologiae Plantarum 35(1):233-239. https://doi.org/10.1016/S0176-1617(11)80240-3

Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, … Perata P (2011). Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479(7373):419-422. https://doi.org/10.1038/nature10536

Li J, Han G, Sun C, Sui N (2019). Research advances of MYB transcription factors in plant stress resistance and breeding. Plant Signaling & Behavior 14(8):1613131. https://doi.org/10.1080/15592324.2019.1613131

Lucas M, Swarup R, Paponov IA, Swarup K, Casimiro I, Lake D, … Wang J (2011). Short-Root regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiology 155(1):384-398. https://doi.org/10.2307/41434010

Mano Y, Omori F, Loaisiga CH, Bird R (2009). QTL mapping of above-ground adventitious roots during waterlogging in maize teosinte Zea nicaraguensis backcross population. Plant Root 3:3-9. https://doi.org/10.3117/plantroot.3.3

Miao LF, Yang F, Han CY, Pu YJ, Ding Y, Zhang LJ (2017). Sex-specific responses to winter flooding, spring waterlogging and post-flooding recovery in Populus deltoides. Science. Reporters 7(1):2534. https://doi.org/10.1038/s41598-017-02765-2

Monika K, Sandro P, Markus S, Friedrich K, Licausi F, Van-Dongen JT (2015). The stability and nuclear localization of the transcription factor RAP2. 12 are dynamically regulated by oxygen concentration. Plant, Cell & Environment 38:1094-1103. https://doi.org/10.1111/pce.12493

Moustakas M, Sperdouli I, Kouna T, Antonopoulou CI, Therios I (2011). Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem ii functioning of Arabidopsis thaliana leaves. Plant Growth Regulation 65(2):315-325. https://doi.org/10.1007/s10725-011-9604-z

Nascimento KJT, Debona D, Rezende D, DaMatta FM, Rodrigues FÁ (2018). Changes in leaf gas exchange and chlorophyll a fluorescence on soybean plants supplied with silicon and infected by Cercospora sojina. Journal of Phytopathology 166 (11-12):747-760. https://doi.org/10.1111/jph.12757

Ohbayashi I, Konishi M, Ebine K, Sugiyama M (2011). Genetic identification of Arabidopsis RID2 as an essential factor involved in pre-rRNA processing. The Plant Journal 67(1):49-60. https://doi.org/10.1111/j.1365-313x.2011.04574.x

Peng Y, Zhou Z, Zhang Z, Yu X, Zhang X, Du K (2018). Molecular and physiological responses in roots of two full-sib poplars uncover mechanisms that contribute to differences in partial submergence tolerance. Scientific Reports 8(1):12829. https://doi.org/10.1038/s41598-018-30821-y

Phukan UJ, Mishra S, Shukla RK (2016). Waterlogging and submergence stress: affect and acclimation. Critical Reviews in Biotechnology 36(5):956-966. https://doi.org/10.3109/07388551.2015.1064856

Rich SM, Ludwig M, Colmer TD (2012). Aquatic adventitious root development in partially and completely submerged wetland plants Cotula coronopifolia and Meionectes brownie. Annals of Botany 110(2):405-414. https://doi.org/10.1093/aob/mcs051

Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, Van-Dongen JT (2010). Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiology 152(3):1501-1513. https://doi.org/10.1104/pp.109.150045

Ruperti B, Botton A, Populin F, Eccher G, Brilli M, Quaggiotti S, Guarracino P, Meggio F (2019). Flooding responses on grapevine: a physiological, transcriptional and metabolic perspective. Frontiers in Plant Science 10:339. https://doi.org/10.3389/fpls.2019.00339

Sairam RK, Dharmar K, Chinnusamy V, Lekshmy S, Joshi R, Bhattacharya P (2011). NADPH oxidase as the source of ROS produced under waterlogging in roots of mung bean. Biologia Plantarum 55(4):746. https://doi.org/10.1007/s10535-011-0179-3

Sasidharan R, Voesenek LA (2015). Ethylene-mediated acclimations to flooding stress. Plant Physiology 169(1):3-12. https://doi.org/10.1104/pp.15.00387

Shabala S, Shabala L, Barcelo J, Poschenrieder C (2014). Membrane transporters mediating root signaling and adaptive responses to oxygen deprivation and soil flooding. Plant, Cell & Environment 37(10):2216-2233. https://doi.org/10.1111/pce.12339

Singh K, Foley RC, Onate-Sanchez L (2002). Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology 5(5):430-436. https://doi.org/10.1016/S1369-5266(02)00289-3

Striker GG, Colmer TD (2017). Flooding tolerance of forage legumes. Journal of Experimental Botany 68(8):1851-1872. https://doi.org/10.1093/jxb/erw239

Tewari S, Arora N, Miransari M (2016). Plant growth promoting rhizobacteria to alleviate soybean growth under abiotic and biotic stresses. In: Abiotic and Biotic Stresses in Soybean Production. Academic Press pp 131-155. https://doi.org/10.1016/B978-0-12-801536-0.00006-2

Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, … Schein J (2006). The genome of black cottonwood, Populus trichocarpa. Science 313(5793):1596-1604. https://doi.org/10.1126/science.1128691.

Valmonte GR, Arthur K, Higgins CM, MacDiarmid RM (2014) Calcium-dependent protein kinases in plants: evolution, expression and function. Plant and Cell Physiology 55(3):551-569. https://doi.org/10.1093/pcp/pct200

Verstraeten I, Beeckman T, Geelen D (2013). Adventitious root induction in Arabidopsis thaliana as a model for in vitro root organogenesis. In: Plant Organogenesis. Humana Press Totowa NJ pp 159-175. https://doi.org/10.1007/978-1-62703-221-6_10

Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010). Hormonal interplay during adventitious root formation in flooded tomato plants. The Plant Journal 63(4):551-562. https://doi.org/10.1111/j.1365-313X.2010.04262.x

Voesenek LACJ, Bailey-Serres J (2013). Waterlogging tolerance: O2 sensing and survival strategies. Current Opinion in Plant Biology 16:647-653. https://doi.org/10.1016/j.pbi.2013.06.008

Wan B, Lin Y, Mou T (2007). Expression of rice Ca2+-dependent protein kinases (CDPKs) genes under different environmental stresses. FEBS Letters 581(6):1179-1189. https://doi.org/10.1016/j.febslet.2007.02.030

Wang Z, Hua J, Yin Y, Gu C, Yu C, Shi Q, ... Yu F (2019). An integrated transcriptome and proteome analysis reveal putative regulators of adventitious root formation in Taxodium ‘Zhongshanshan’. International Journal of Molecular Sciences 20(5):12-25. https://doi.org/10.3390/ijms20051225

Waszczak C, Carmody M, Kangasjärvi J (2018). Reactive oxygen species in plant signaling. Annual Review of Plant Biology 69:209-236. https://doi.org/10.1146/annurev-arplant-042817-040322

Wellburn, Alan R (1994). The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144(3):307-313. https://doi.org/10.1016/S0176-1617(11)81192-2

Xu J, Tian YS, Peng RH, Xiong AS, Zhu B, Jin XF, Yao QH (2010). AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis. Planta 231(6):1251-1260. https://doi.org/10.2307/23391490

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 Biology 17(1):1-13. https://doi.org/10.1186/s12870-017-1081-8

Yamauchi T, Watanabe K, Fukazawa A, Mori H, Abe F, Kawaguchi K, Oyanagi A, Nakazono M (2014). Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions. Journal of Experimental Botany 65(1):261-273. https://doi.org/10.1093/jxb/ert371

Yang F, Wang Y, Wang J, Deng WQ, Liao L, Li M (2011). Different ecophysiological responses between male and female Populus deltoides clones to waterlogging stress. Forest Ecology and Management 262(11):1963-1971. https://doi.org/10.1016/j.foreco.2011.08.039

Yang F, Xu X, Xiao X, Li C (2009). Responses to drought stress in two poplar species originating from different altitudes. Biologia Plantarum 53(3):511-516. https://doi.org/10.1007/s10535-009-0092-1

Yang O, Popova OV, Süthoff U, Lüking I, Dietz KJ, Golldack D (2009). The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance. Gene 436(1-2):45-55. https://doi.org/10.1016/j.gene.2009.02.010

Yan K, Zhao S, Cui M, Han G, Wen P (2018). Vulnerability of photosynthesis and photosystem I in Jerusalem artichoke (Helianthus tuberosus L.) exposed to waterlogging. Plant Physiology and Biochemistry 125:239-246. https://doi.org/10.1016/j.plaphy.2018.02.017

Zabalza A, Van-Dongen JT, Froehlich A, Oliver SN, Faix B, Gupta KJ, … Geigenberger P (2009). Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiology 149(2):1087-1098. https://doi.org/10.1104/pp.108.129288

Zhang Q, Huber H, Beljaars SJ, Birnbaum D, de Best S, de Kroon H, Visser EJ (2017). Benefits of flooding-induced aquatic adventitious roots depend on the duration of submergence: linking plant performance to root functioning. Annals of Botany 120(1):171-180. https://doi.org/10.1093/aob/mcx049

Zhou Z, Li G, Sun X, Xu F, Chen Z (2019). Physiological responses and tolerance evaluation of five poplar varieties to waterlogging. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 47(3):658-667. https://doi.org/10.15835/nbha47311440

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. Royal Society Open Science 5(6):172253. https://doi.org/10.1098/rsos.172253

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2020-09-14

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LI, G., FU, Q., LIU, Z., YE, J., ZHANG, W., LIAO, Y., XU, F., & ZHOU, Z. (2020). Understanding physiological and molecular mechanisms of Populus deltoides ‘DanHongYang’ tolerance to waterlogging by comparative transcriptome analysis. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 48(3), 1613–1636. https://doi.org/10.15835/nbha48311977

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Vol. 48 No. 3 (2020)

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Research Articles
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DOI: 10.15835/nbha48311977

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