Abstract
Waterlogging is a major abiotic stress limiting crop growth and yield. There is a distinct difference among cereal crops in their responses to waterlogging stress, however, little is known about the mechanisms underlying waterlogging tolerance. Here, we investigated the influence of waterlogging stress on seedling growth and physiological traits of three cereal plants with distinct waterlogging tolerance, i.e. sea barley (Hordeum marinum, H559), wheat (Triticum aestivum, Chinese Spring) and barley (Hordeum vulgare, ZU9). Sea barley is much stronger in waterlogging-tolerance than wheat, with barley being the least. Under waterlogging biomass, shoot and root length, contents of chlorophyll and soluble protein were significantly reduced, and MDA content and POD activity were significantly increased in barley and wheat seedlings in comparison with the control, but these parameters remained little change in sea barley under waterlogging in comparison with the control. Expression levels of hypoxia-responding related genes, such as ADH1, XET1 and ERF1 were more induced under waterlogging treatment in sea barley than those in wheat and barley. Constitutive aerenchyma could be observed in the roots of sea barley under normal condition, and aerenchyma was more developed under waterlogging. However, there was no aerenchyma in the roots of barley and wheat in both control and waterlogging treatments. Obviously, higher waterlogging tolerance in sea barley could be attributed to its constitutive and induced aerenchyma.
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Abbreviations
- ACO:
-
1-Aminocyclopropane-1-carboxylic acid oxidase
- ADH1:
-
Alcohol dehydrogenase 1
- ARs:
-
Adventitious roots
- CAT:
-
Catalase
- CC:
-
Chlorophyll content
- DW:
-
Dry weight
- ERF1:
-
Ethylene-responsive factor 1
- FW:
-
Fresh weight
- LDH1:
-
Lactate dehydrogenase 1
- MC:
-
MDA content
- MDA:
-
Malondialdehyde
- NR:
-
Nitrate reductase
- NRA:
-
Nitrate reductase activity
- PA:
-
POD activity
- PDC1:
-
Pyruvate decarboxylase 1
- POD:
-
Peroxidase
- RAP2.3:
-
Related to apetala2.3
- RDW:
-
Root dry weight
- RFW:
-
Root fresh weight
- RRWC:
-
Root relative water content
- RL:
-
Root length
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
- SAUR:
-
Small auxin up RNA
- SDW:
-
Shoot dry weight
- SFW:
-
Shoot fresh weight
- SL:
-
Shoot length
- SOD:
-
Superoxide dismutase
- SPAD:
-
Soil plant analysis development
- SPC:
-
Soluble protein content
- SRWC:
-
Shoot relative water content
- XET:
-
Xyloglucan endotransglycosylase
References
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. Sci Rep 7:10950
Bailey-Serres J, Colmer TD (2014) Plant tolerance of flooding stress–recent advances. Plant Cell Environ 37:2211–2215
Borrego-Benjumea A, Carter A, Tucker JR, Yao Z, Xu W, Badea A (2020) Genome-wide analysis of gene expression provides new insights into waterlogging responses in barley (Hordeum vulgare L.). Plants 9:240
Borrego-Benjumea A, Carter A, Zhu M, Tucker JR, Zhou MX, Badea A (2021) Genome-wide association study of waterlogging tolerance in barley (Hordeum vulgare L.) under controlled field conditions. Front Plant Sci 12:711654
Carmona A, Friero E, Bustos AD, Jouve N, Cuadrado A (2013) The evolutionary history of sea barley (Hordeum marinum) revealed by comparative physical mapping of repetitive DNA. Ann Bot 112:1845–1855
Chen S, Xu ZY, Adil MF, Zhang GP (2021) Cultivar-, stress duration- and leaf age-specific hub genes and co-expression networks responding to waterlogging in barley. Environ Exp Bot 191:104599
Das KK, Panda D, Sarkar RK, Reddy JN, Ismail AM (2009) Submergence tolerance in relation to variable floodwater conditions in rice. Environ Exp Bot 66:425–434
De San Celedonio RP, Abeledo LG, Miralles DJ (2018) Physiological traits associated with reductions in grain number in wheat and barley under waterlogging. Plant Soil 429:469–481
Eysholdt-Derzso E, Sauter M (2017) Root bending is antagonistically affected by hypoxia and ERF-mediated transcription via auxin signaling. Plant Physiol 175:412–423
Farooq A, Bukhari SA, Akram NA, Ashraf M, Wijaya L, Alyemeni MN (2020) Exogenously applied ascorbic acid-mediated changes in osmoprotection and oxidative defense system enhanced water stress tolerance in different cultivars of safflower (Carthamus tinctorious L.). Plants Basel 9:104
Fu LB, Shen QF, Kuang LH, Wu DZ, Zhang GP (2019) Transcriptomic and alternative splicing analyses reveal mechanisms of the difference in salt tolerance between barley and rice. Environ Exp Bot 166:103810
Garthwaite AJ, von Bothmer R, Colmer TD (2003) Diversity in root aeration traits associated with waterlogging tolerance in the genus Hordeum. Funct Plant Biol 30:875–889
Hirabayashi Y, Mahendran R, Koirala S, Konoshima L, Yamazaki D, Watanabe S, Kim H, Kanae S (2013) Global flood risk under climate change. Nat Clim Change 3:816–821
Huang L, Kuang LH, Li X, Wu LY, Wu DZ, Zhang GP (2018) Metabolomic and transcriptomic analyses reveal the reasons why Hordeum marinum has higher salt tolerance than Hordeum vulgare. Environ Exp Bot 156:48–61
Islam S, Malik AI, Islam A, Colmer TD (2007) Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents. J Exp Bot 58:1219–1229
Jiang D, Fan XM, Dai TB, Cao WX (2008) Nitrogen fertiliser rate and post-anthesis waterlogging effects on carbohydrate and nitrogen dynamics in wheat. Plant Soil 304:301–304
Jimenez JD, Clode PL, Signorelli S, Veneklaas EJ, Colmer TD, Kotula L (2021) The barrier to radial oxygen loss impedes the apoplastic entry of iron into the roots of Urochloa humidicola. J Exp Bot 72:3279–3293
Kaur G, Sharma P, Rathee S, Singh HP, Batish DR, Kohli RK (2021a) Salicylic acid pre-treatment modulates Pb2+-induced DNA damage vis-à-vis oxidative stress in Allium cepa roots. Environ Sci Pollut Res 28:51989–52000
Kaur K, Goyal K, Arora K, Kaur G (2021b) Genotypic variations in nitrate respiration along with potassium nitrate treatment - accountable for waterlogging tolerance in maize. Biologia 76:1651–1660
Kreuzwieser J, Rennenberg H (2015) Molecular and physiological responses of trees to waterlogging stress. Plant Cell Environ 37:2245–2259
Kumar R, Singh V, Pawar SK, Singh PK, Kaur A, Sharma D (2019) Abiotic Stress and Wheat Grain Quality: A Comprehensive Review. In: Hasanuzzaman M, Nahar K, Hossain M (eds) Wheat Production in Changing Environments. Springer, Singapore, pp 63–87
Li CY, Liu DC, Lin Z, Guan B, Liu D, Yang L, Deng XY, Mei FZ, Zhou ZQ (2019) Histone acetylation modification affects cell wall degradation and aerenchyma formation in wheat seminal roots under waterlogging. Plant Growth Regul 87:149–163
Liu MY, Hulting A, Mallory-Smith C (2017) Comparison of growth and physiological characteristics between roughstalk bluegrass and tall fescue in response to simulated waterlogging. PLoS One 12:e0182035
Liu Q, Dong GR, Ma YQ, Huang XX, Mu TJ, Huang XX, Li YJ, Li XG, Hou BK (2021) Glycosyltransferase UGT79B7 negatively regulates hypoxia response through γ-aminobutyric acid homeostasis in Arabidopsis. J Exp Bot 107:1093–1105
Lorbiecke R, Sauter M (1999) Adventitious root growth and cell-cycle induction in deep water rice. Plant Physiol 119:21–29
Loreti E, van Veen H, Perata P (2016) Plant responses to flooding stress. Curr Opin Plant Biol 33:64–71
Luan HY, Shen HQ, Pan YH, Guo BJ, Chao L, Xu RG (2018) Elucidating the hypoxic stress response in barley (Hordeum vulgare L.) during waterlogging: A proteomics approach. Sci Rep 8:9655
Luan HY, Guo BJ, Shen HQ, Pan YH, Hong Y, Chao L, Xu RG (2020) Overexpression of barley transcription factor HvERF2.11 in Arabidopsis enhances plant waterlogging tolerance. Int J Mol Sci 21:1982
Lucie M, Pavel V, Radovan H, Prášil IT, Klára K (2016) Proteomic response of Hordeum vulgare cv. Tadmor and Hordeum marinum to salinity stress: similarities and differences between a glycophyte and a halophyte. Front Plant Sci 7:1154
Malik AI, Colmer TD, Lambers H, Schortemeyer M (2003) Aerenchyma formation and radial O2 loss along adventitious roots of wheat with only the apical root portion exposed to O2 deficiency. Plant Cell Environ 26:1713–1722
Masoni A, Pampana S, Arduini I (2016) Barley response to waterlogging duration at tillering. Crop Sci 56:2722–2730
McDonald MP, Galwey NW, Colmer TD (2001) Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss. Plant Cell Environ 24:585–596
Pampana S, Masoni A, Arduini I (2016) Grain yield of durum wheat as affected by waterlogging at tillering. Cereal Res Commun 44:706–716
Parent C, Nicolas C, Audrey B, Crevècoeur M, Dat J (2008) An overview of plant responses to soil waterlogging. Plant Stre 2:20–27
Ploschuk RA, Miralles DJ, Colmer TD, Ploschuk EL, Striker GG (2018) Waterlogging of winter crops at early and late stages: impacts on leaf physiology, growth and yield. Front Plant Sci 9:1863
Qi XH, Li T, Xu Q, Chen XH (2011) Modulation of chlorophyll contents and anti-oxidant systems in two cucumber varieties under waterlogging stress and subsequent drainage. J Hortic Sci Biotech 86:337–342
Qi XH, Li QQ, Ma XT, Qian CL, Wang HH, Ren NN, Shen CX, Huang SM, Xu XW, Xu Q, Chen XH (2019) Waterlogging-induced adventitious root formation in cucumber is regulated by ethylene and auxin through reactive oxygen species signaling. Plant Cell Environ 42:1458–1470
Ren H, Gray WM (2015) SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant 8:1153–1164
Romina P, Abeledo LG, Miralles DJ (2014) Identifying the critical period for waterlogging on yield and its components in wheat and barley. Plant Soil 378:265–277
Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant Soil 253:1–34
Shen QF, Fu LB, Qiu L, Feng X, Zhang GP, Wu DZ (2016) Time-course of ionic responses and proteomic analysis of a Tibetan wild barley at early stage under salt stress. Plant Growth Regul 81:11–21
Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170:603–617
Striker GG, Colmer TD (2017) Flooding tolerance of forage legumes. J Exp Bot 68:1851–1872
Sundgren TK, Uhlen AK, Waalen W, Lillemo M (2018) Field screening of waterlogging tolerance in spring wheat and spring barley. Agron 8:38
Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63:551–562
Voesenek LACJ, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytol 206:57–73
Wang BD (2006) Cultural eutrophication in the Changjiang (Yangtze River) plume: history and perspective. Estuar Coast Shelf S 69:471–477
Wang NB, Zhao J, He XY, Sun HY, Zhang GP, Wu FB (2015) Comparative proteomic analysis of drought tolerance in the two contrasting Tibetan wild genotypes and cultivated genotype. BMC Genomics 16:432
Westra S, Fowler HJ, Evans JP, Alexander LV, Berg P, Johnson F, Kendon EJ, Lenderink Roberts NM (2014) Future changes to the intensity and frequency of short-duration extreme rainfall: future intensity of sub-daily rainfall. Rev Geophy 52:522–555
Wu WM, Chen HJ, Wang SJ, Wei FZ, Li JC (2015) Effects of nitrogen fertilization application regime on dry matter, nitrogen accumulation and transportation in summer maize under waterlogging at the seedling stage. Acta Agron Sin 41:1246–1256
Xie RJ, Zheng L, Jiao Y, Huang X (2021) Understanding physiological and molecular mechanisms of citrus rootstock seedlings in response to root zone hypoxia by RNA-Seq. Environ Exp Bot 192:104647
Xu XW, Ji J, Ma XT, Xu Q, Qi XH, Chen XH (2016) Comparative proteomic analysis provides insight into the key proteins involved in cucumber (Cucumis sativus L.) adventitious root emergence under waterlogging stress. Front Plant Sci 7:1515
Xu L, Pan R, Shabala L, Shabala S, Zhang WY (2019) Temperature influences waterlogging stress-induced damage in Arabidopsis through the regulation of photosynthesis and hypoxia-related genes. Plant Growth Regul 89:143–152
Yaduvanshi N, Setter T, Sharma S, Singh K, Kulshreshtha N (2014) Influence of waterlogging on yield of wheat (Triticum aestivum), redox potentials, and concentrations of microelements in different soils in India and Australia. Soil Res 50:489–499
Yu B, Zhao CY, Li J, Li JY, Peng G (2015) Morphological, physiological, and biochemical responses of Populus euphratica to soil flooding. Photosynthetica 53:110–117
Zhang XC, Shabala S, Koutoulis A, Shabala L, Johnson P, Hayes D, Nichols DS, Zhou MX (2015) Waterlogging tolerance in barley is associated with faster aerenchyma formation in adventitious roots. Plant Soil 394:355–372
Zhang JY, Huang SN, Chen YH, Wang G, Guo ZR (2017) Identification and characterization of two waterlogging responsive alcohol dehydrogenase genes (AdADH1 and AdADH2) in Actinidia deliciosa. Mol Breed 37:52–65
Zhou WG, Chen F, Meng YJ, Chandrasekaran U, Luo XF, Yang WY, Shu K (2020) Plant waterlogging/flooding stress responses: From seed germination to maturation. Plant Physiol Bioch 148:228–236
Acknowledgements
This work was supported by Natural Science Foundation of China (32171929, 31901429), China Agriculture Research System (CARS-05), Key Research Projects of Zhejiang Province (2021C02057) and Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP).
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Xu, Z., Shen, Q. & Zhang, G. The mechanisms for the difference in waterlogging tolerance among sea barley, wheat and barley. Plant Growth Regul 96, 431–441 (2022). https://doi.org/10.1007/s10725-021-00789-3
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DOI: https://doi.org/10.1007/s10725-021-00789-3