Abstract
To cope with flooding-induced hypoxia, plants have evolved different strategies. Molecular strategies, such as the N-degron pathway and transcriptional regulation, are known to be crucial for Arabidopsis thaliana’s hypoxia response. Our study uncovered a novel molecular strategy that involves a single transcription factor interacting with two identical cis-elements, one located in the promoter region and the other within the intron. This unique double-element adjustment mechanism has seldom been reported in previous studies. In humid areas, WRKY70 plays a crucial role in A. thaliana’s adaptation to submergence-induced hypoxia by binding to identical cis-elements in both the promoter and intron regions of WRKY33. This dual binding enhances WRKY33 expression and the activation of hypoxia-related genes. Conversely, in arid regions lacking the promoter cis-element, WRKY70 only binds to the intron cis-element, resulting in limited WRKY33 expression during submergence stress. The presence of a critical promoter cis-element in humid accessions, but not in dry accessions, indicates a coordinated regulation enabling A. thaliana to adapt and thrive in humid habitats.
Key message
A coordination strategy between two cis-elements of WRKY33 regulated by the same transcription factor, WRKY70, promotes humid adaption of A. thaliana.
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References
Abbas M, Sharma G, Dambire C, Marquez J, Alonso-Blanco C, Proaño K, Holdsworth MJ (2022) An oxygen-sensing mechanism for angiosperm adaptation to altitude. Nature 606(7914):565–569
Bailey-Serres J, Voesenek LACJ (2008) Flooding stress, acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339
Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LACJ, van Dongen JT (2012a) Making sense of low oxygen sensing. Trends Plant Sci 17:129–138
Bailey-Serres J, Lee SC, Brinton E (2012b) Waterproofing crops: effective flooding survival strategies. Plant Physiol 160:1698–1709
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M, Paszkowski J (2004) Chromatin techniques for plant cells. Plant J 39:776–789
Chen J, Nolan TM, Ye H, Zhang M, Tong H, Xin P, Chu J, Chu C, Li Z, Yin Y (2017) Arabidopsis WRKY46, WRKY54, and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought responses. Plant Cell 29:1425–1439
Chen S, Ding Y, Tian H, Wang S, Zhang Y (2021) WRKY54 and WRKY70 positively regulate SARD1 and CBP60g expression in plant immunity. Plant Signal Behav 16:1932142
Cho HY, Wen TN, Wang YT, Shih MC (2016) Quantitative phosphoproteomics of protein kinase SnRK1 regulated protein phosphorylation in Arabidopsis under submergence. J Exp Bot 67:2745–2760
Cui W, Chen Z, Shangguan X, Li T, Wang L, Xue X, Cao J (2022) TRY intron2 determined its expression in inflorescence activated by SPL9 and MADS-box genes in Arabidopsis. Plant Sci 321:111311
Fick SE, Hijmans RJ (2017) WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315
Gasch P, Fundinger M, Muller JT, Lee T, Bailey-Serres J, Mustroph A (2016) Redundant ERF-VII transcription factors bind to an evolutionarily conserved cis-Motif to regulate hypoxia-responsive gene expression in Arabidopsis. Plant Cell 28:160–180
Genomes Consortium (2016) 1,135 genomes reveal the global pattern of polymorphism in Arabidopsis thaliana. Cell 166:481–491
Gibbs DJ, Holdsworth MJ (2020) Every breath you take: new insights into plant and animal oxygen sensing. Cell 180:22–24
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 479:415–418
Giuntoli B, Lee SC, Licausi F, Kosmacz M, Oosumi T, van Dongen JT, Bailey-Serres J, Perata P (2014) A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis. PLoS Biol 12:e1001950
Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030
Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494
Kosarev P, Mayer KFX, Hardtke CS (2002) Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol 3:RESEARCH0016
Li Z, Fu D, Wang X, Zeng R, Zhang X, Tian J, Zhang S, Yang X, Tian F, Lai J, Shi Y, Yang S (2022) The transcription factor bZIP68 negatively regulates cold tolerance in maize. Plant Cell 34:2833–2851
Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, Perata P, Van Dongen JT (2011a) Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479:419–422
Licausi F, Weits DA, Pant BD, Scheible WR, Geigenberger P, van Dongen JT (2011b) Hypoxia responsive gene expression is mediated by various subsets of transcription factors and miRNAs that are determined by the actual oxygen availability. New Phytol 190:442–456
Liu B, Jiang Y, Tang H, Tong S, Lou S, Shao C, Zhang J, Song Y, Chen N, Bi H, Zhang H, Li J, Liu J, Liu H (2021a) The ubiquitin E3 ligase SR1 modulates the submergence response by degrading phosphorylated WRKY33 in Arabidopsis. Plant Cell 33:1771–1789
Liu H, Liu B, Lou S, Bi H, Tang H, Tong S, Song Y, Chen N, Zhang H, Jiang Y, Liu J (2021b) CHYR1 ubiquitinates the phosphorylated WRKY70 for degradation to balance immunity in Arabidopsis thaliana. New Phytol 230:1095–1109
Lou S, Guo X, Liu L, Song Y, Zhang L, Jiang Y, Zhang L, Sun P, Liu B, Tong S, Chen N, Liu M, Zhang H, Liang R, Feng X, Zheng Y, Liu H, Holdsworth MJ, Liu J (2022) Allelic shift in cis-elements of the transcription factor RAP212 underlies adaptation associated with humidity in Arabidopsis thaliana. Sci Adv 8:eabn8281
Machens F, Becker M, Umrath F, Hehl R (2014) Identification of a novel type of WRKY transcription factor binding site in elicitor-responsive cis-sequences from Arabidopsis thaliana. Plant Mol Biol 84:371–385
Meng X (2019) The role of mitochondrial function and retrograde signalling for stress responses in Arabidopsis thaliana. La Trobe University, Melbourne
Meng F, Zhao H, Zhu B, Zhang T, Yang M, Li Y, Han Y, Jiang J (2021) Genomic editing of intronic enhancers unveils their role in fine-tuning tissue-specific gene expression in Arabidopsis thaliana. Plant Cell 33:1997–2014
Métraux JP, Kende H (1983) The role of ethylene in the growth response of submerged deep water rice. Plant Physiol 72:441–446
Nagai K, Hattori Y, Ashikari M (2010) Stunt or elongate? Two opposite strategies by which rice adapts to floods. J Plant Res 123:303–309
Raskin I, Kende H (1984) Role of gibberellin in the growth response of submerged deep water rice. Plant Physiol 76:947–950
Rhine MD, Stevens G, Shannon G, Wrather A, Sleper D (2010) Yield and nutritional responses to waterlogging of soybean cultivars. Irrig Sci 28:135–142
Santuari L, Sanchez-Perez GF, Luijten M, Rutjens B, Terpstra I, Berke L, Gorte M, Prasad K, Bao D, Timmermans-Hereijgers JLPM, Maeo K, Nakamura K, Shimotohno A, Pencik A, Novak O, Ljung K, van Heesch S, de Bruijn E, Cuppen E, Willemsen V, Mähönen AP, Lukowitz W, Snel B, de Ridder D, Scheres B, Heidstra R (2016) The PLETHORA gene regulatory network guides growth and cell differentiation in Arabidopsis roots. Plant Cell 28:2937–2951
Sasidharan R, Bailey-Serres J, Ashikari M, Atwell BJ, Colmer TD, Fagerstedt K, Fukao T, Geigenberger P, Hebelstrup KH, Hill RD, Holdsworth MJ, Ismail AM, Licausi F, Mustroph A, Nakazono M, Pedersen O, Perata P, Sauter M, Shih MC, Sorrell BK, Striker GG, van Dongen JT, Whelan J, Xiao S, Visser EJW, Voesenek LACJ (2017) Community recommendations on terminology and procedures used in flooding and low oxygen stress research. New Phytol 214:1403–1407
Singh P, Sinha AK (2016) A positive feedback loop governed by SUB1A1 interaction with MITOGEN-ACTIVATED PROTEIN KINASE3 imparts submergence tolerance in rice. Plant Cell 28:1127–1143
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 223:604–612
Tang H, Bi H, Liu B, Lou S, Song Y, Tong S, Chen N, Jiang Y, Liu J, Liu H (2021) WRKY33 interacts with WRKY12 protein to up-regulate RAP2.2 during submergence induced hypoxia response in Arabidopsis thaliana. New Phytol 229:106–125
Trabucco A, Zomer RJ (2009) Global aridity index (Global-Aridity) and global potential evapo-transpiration (Global-PET) geospatial database. (CGIAR Consortium for Spatial Information); http://www.csi.cgiar.org
Vashisht D, Hesselink A, Pierik R, Ammerlaan JM, Bailey-Serres J, Visser EJ, Pedersen O, van Zanten M, Vreugdenhil D, Jamar DC, Voesenek LA, Sasidharan R (2011) Natural variation of submergence tolerance among Arabidopsis thaliana accessions. New Phytol 190:299–310
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 JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749
Weits DA, Giuntoli B, Kosmacz M, Parlanti S, Hubberten H-M, Riegler H, Hoefgen R, Perata P, Van Dongen JT, Licausi F (2014) Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway. Nat Commun 5:3425
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2:e718
Yang CY, Hsu FC, Li JP, Wang NN, Shih MC (2011) The AP2/ERF transcription factor AtERF73/HRE1 modulates ethylene responses during hypoxia in Arabidopsis. Plant Physiol 156:202–212
Yu N, Cai WJ, Wang S, Shan CM, Wang LJ, Chen XY (2010) Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22:2322–2335
Zhai N, Xu L (2021) Pluripotency acquisition in the middle cell layer of callus is required for organ regeneration. Nat Plants 7:1453–1460
Zhang C, Xu Y, Guo S, Zhu J, Huan Q, Liu H, Wang L, Luo G, Wang X, Chong K (2012) Dynamics of brassinosteroid response modulated by negative regulator LIC in rice. PLoS Genet 8:e1002686
Acknowledgements
Thanks to these fundings (the National Natural Science Foundation of China No. 32270302 and No. 32030006, the Strategic Priority Research Program of Chinese Academy of Sciences XDB31010300 and the Fundamental Research Funds for the Central Universities SCU2022D003) for their support. Thanks to ABRC for providing the mutant seeds used in this work.
Funding
This research was supported by the National Natural Science Foundation of China (Grant Nos. 32270302, 32030006, and 31670317), the Strategic Priority Research Program of Chinese Academy of Sciences (Grant No. XDB31010300), and the Fundamental Research Funds for the Central Universities (2020SCUNL207, SCU2019D013).
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L.H.H., L.B. and Z.Y.D. designed the research. L.B., Z.Y.D., L.H.H., L.S.L., L.M., W.W.W., F.X.Q and Z.H carried out the experiments. L.B. and Z.Y.D. analyzed the data. L.H.H. and L.B. wrote and revised the article.
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Sequence data from this article can be found in the Arabidopsis Genome Initiative or GenBank/EMBL databases under the following accession numbers: WRKY70 (AT3G56400), WRKY33 (AT2G38470), SR1 (AT2G47090), ADH1 (AT1G77120), PDC1 (AT4G33070), SUS4 (AT3G43190), PCO2 (AT5G39890), HB1 (AT2G16060), ACS2 (AT1G01480), WRKY12 (AT2G44745), IRX3 (AT5G17420), CAT2 (AT1G58030), WAK2 (AT1G21270), RAP2.2 (AT3G14230), AT1G66810 and AT5G22920.
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Liu, B., Zheng, Y., Lou, S. et al. Coordination between two cis-elements of WRKY33, bound by the same transcription factor, confers humid adaption in Arabidopsis thaliana. Plant Mol Biol 114, 30 (2024). https://doi.org/10.1007/s11103-024-01428-x
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DOI: https://doi.org/10.1007/s11103-024-01428-x