Abstract
Main Conclusion
OsRR26 is a cytokinin-responsive response regulator that promotes phytohormone-mediated ROS accumulation in rice roots, regulates seedling growth, spikelet fertility, awn development, represses NADPH oxidases, and negatively affects salinity tolerance.
Plant two-component systems (TCS) play a pivotal role in phytohormone signaling, stress responses, and circadian rhythm. However, a significant knowledge gap exists regarding TCS in rice. In this study, we utilized a functional genomics approach to elucidate the role of OsRR26, a type-B response regulator in rice. Our results demonstrate that OsRR26 is responsive to cytokinin, ABA, and salinity stress, serving as the ortholog of Arabidopsis ARR11. OsRR26 primarily localizes to the nucleus and plays a crucial role in seedling growth, spikelet fertility, and the suppression of awn development. Exogenous application of cytokinin led to distinct patterns of reactive oxygen species (ROS) accumulation in the roots of both WT and transgenic plants (OsRR26OE and OsRR26KD), indicating the potential involvement of OsRR26 in cytokinin-mediated ROS signaling in roots. The application of exogenous ABA resulted in varied cellular compartmentalization of ROS between the WT and transgenic lines. Stress tolerance assays of these plants revealed that OsRR26 functions as a negative regulator of salinity stress tolerance across different developmental stages in rice. Physiological and biochemical analyses unveiled that the knockdown of OsRR26 enhances salinity tolerance, characterized by improved chlorophyll retention and the accumulation of soluble sugars, K+ content, and amino acids, particularly proline.
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Abbreviations
- HK:
-
Histidine kinase
- H2DCFDA:
-
2,7-dichlorodihydrofluorescein diacetate
- ROS:
-
Reactive oxygen species
- RR:
-
Response regulator
- SOD:
-
Superoxide dismutase
- TCS:
-
Two component signaling
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, Etheridge N, Argyros DA, Mason MG, Kieber JJ, Schaller GE (2008) Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20(8):2102–2116. https://doi.org/10.1105/tpc.108.059584
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Chen CW, Yang YW, Lur HS, Tsai YG, Chang MC (2006) A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development. Plant Cell Physiol 47(1):1–13. https://doi.org/10.1093/pcp/pci216
Choi J, Lee J, Kim K, Cho M, Ryu H, An G, Hwang I (2012) Functional identification of OsHk6 as a homotypic cytokinin receptor in rice with preferential affinity for iP. Plant Cell Physiol 53(7):1334–1343. https://doi.org/10.1093/pcp/pcs079
Choudhary A, Kumar A, Kaur N (2020) ROS and oxidative burst: roots in plant development. Plant Divers 42(1):33–43. https://doi.org/10.1016/j.pld.2019.10.002
Ding W, Tong H, Zheng W, Ye J, Pan Z, Zhang B, Zhu S (2017) Isolation, characterization and transcriptome analysis of a cytokinin receptor mutant osckt1 in rice. Front Plant Sci 8:88. https://doi.org/10.3389/fpls.2017.00088
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 59(2):315–318. https://doi.org/10.1104/pp.59.2.315
Grefen C, Harter K (2004) Plant two-component systems: principles, functions, complexity and cross talk. Planta 219:733–742. https://doi.org/10.1007/s00425-004-1316-4
Gregorio GB, Senadhira D, Mendoza RD (1997) Screening rice for salinity tolerance. In: IRRI Discussion Paper Series No. 22. lnternational Rice Research Institute, Manila (Philippines) 2169-2019-1605
Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102. https://doi.org/10.1023/A:1005703923347
Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and O2•-/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127(3):817–831. https://doi.org/10.1104/pp.010188
Hua L, Wang DR, Tan L et al (2015) LABA1, a domestication gene associated with long, barbed awns in wild rice. Plant Cell 27(7):1875–1888. https://doi.org/10.1105/tpc.15.00260
Huang Y, Zhou J, Li Y, Quan R, Wang J, Huang R, Qin H (2021) Salt stress promotes abscisic acid accumulation to affect cell proliferation and expansion of primary roots in rice. Int J Mol Sci 22(19):10892. https://doi.org/10.3390/ijms221910892
Imamura A, Kiba T, Tajima Y, Yamashino T, Mizuno T (2003) In vivo and in vitro characterization of the ARR11 response regulator implicated in the His-to-Asp phosphorelay signal transduction in Arabidopsis thaliana. Plant Cell Physiol 44(2):122–131. https://doi.org/10.1093/pcp/pcg014
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8(3):275–282. https://doi.org/10.1093/bioinformatics/8.3.275
Karan R, Singla-Pareek SL, Pareek A (2009) Histidine kinase and response regulator genes as they relate to salinity tolerance in rice. Funct Integr Genomics 9:411–417. https://doi.org/10.1007/s10142-009-0119-x
Kikkert JR (1993) The Biolistic® PDS-1000/He device. Plant Cell Tissue Organ Cult 33:221–226. https://doi.org/10.1007/BF02319005
Koyro HW, Ahmad P, Geissler N (2012) Abiotic stress responses in plants: an overview. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 1–28
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Kushwaha HR, Singla-Pareek SL, Pareek A (2014) Putative osmosensor-OsHK3b-a histidine kinase protein from rice shows high structural conservation with its ortholog AtHK1 from Arabidopsis. J Biomol Struct Dyn 32(8):1318–1332. https://doi.org/10.1080/07391102.2013.818576
Lakra N, Kaur C, Anwar K, Singla-Pareek SL, Pareek A (2018) Proteomics of contrasting rice genotypes: identification of potential targets for raising crops for saline environment. Plant Cell Environ 41(5):947–969. https://doi.org/10.1111/pce.12946
Li T, Yang S, Kang X, Lei W, Qiao K, Zhang D, Lin H (2019) The bHLH transcription factor gene AtUPB1 regulates growth by mediating cell cycle progression in Arabidopsis. Biochem Biophys Res Commun 518(3):565–572. https://doi.org/10.1016/j.bbrc.2019.08.088
Li C, Gong C, Wu J, Yang L, Zhou L, Wu B, Gao L, Ling F, You A, Li C, Lin Y (2022) Improvement of rice agronomic traits by editing type-B response regulators. Int J Mol Sci 23(22):14165. https://doi.org/10.3390/ijms232214165
Liu Y, Peng X, Ma A, Liu W, Liu B, Yun J-D, Xu Z-Y (2023) Type-B response regulator OsRR22 forms a transcriptional activation complex with OsSLR1 to modulate OsHKT2;1 expression in rice. Sci China Life Sci 66:2922–2934. https://doi.org/10.1007/s11427-023-2464-2
Lohrmann J, Harter K (2002) Plant two-component signaling systems and the role of response regulators. Plant Physiol 128(2):363–369. https://doi.org/10.1007/s00425-004-1316-4
López-Hidalgo C, Meijón M, Lamela L, Valledor L (2021) The rainbow protocol: a sequential method for quantifying pigments, sugars, free amino acids, phenolics, flavonoids and MDA from a small amount of sample. Plant Cell Environ 44(6):1977–1986. https://doi.org/10.1111/pce.14007
Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, Hao F (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63(1):305–317. https://doi.org/10.1093/jxb/err280
Mase K, Tsukagoshi H (2021) Reactive oxygen species link gene regulatory networks during Arabidopsis root development. Front Plant Sci 12:660274. https://doi.org/10.3389/fpls.2021.660274
Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, Alonso JM, Ecker JR, Schaller GE (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17(11):3007–3018. https://doi.org/10.1105/tpc.105.035451
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Murakeozy EP, Nagy Z, Duhaze C, Bouchereau A, Tuba Z (2003) Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary. J Plant Physiol 160:395–401
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880
Naruse M, Takahashi H, Kurata N, Ito Y (2018) Cytokinin-induced expression of OSH1 in a shoot-regenerating rice callus. Plant Biotechnol 35(3):267–272. https://doi.org/10.5511/plantbiotechnology.18.0614a
Nguyen KH, Van Ha C, Nishiyama R, Watanabe Y, Leyva-González MA, Fujita Y, Tran UT, Li W, Tanaka M, Seki M, Schaller GE (2016) Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc Natl Acad Sci USA 113(11):3090–3095. https://doi.org/10.1073/pnas.1600399113
Nongpiur R, Soni P, Karan R, Singla-Pareek SL, Pareek A (2012) Histidine kinases in plants: cross talk between hormone and stress responses. Plant Signal Behav 7(10):1230–1237. https://doi.org/10.4161/psb.21516
Nongpiur RC, Gupta P, Sharan A, Singh D, Singla-Pareek SL, Pareek A (2019) The two-component system: transducing environmental and hormonal signals. In: Sopory S (ed) Sensory biology of plants. Springer, Singapore, pp 247–278
Pareek A, Singh A, Kumar M, Kushwaha HR, Lynn AM, Singla-Pareek SL (2006) Whole-genome analysis of Oryza sativa reveals similar architecture of two-component signaling machinery with Arabidopsis. Plant Physiol 142(2):380–397. https://doi.org/10.1104/pp.106.086371
Rejeb KB, Lefebvre-De Vos D, Le DI, Leprince A-S, Bordenave M, Maldiney R, Jdey A, Abdelly C, Savoure A (2015) Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol 208(4):1138–1148. https://doi.org/10.1111/nph.13550
Sahoo KK, Tripathi AK, Pareek A, Sopory SK, Singla-Pareek SL (2011) An improved protocol for efficient transformation and regeneration of diverse indica rice cultivars. Plant Methods 7(1):1–11. https://doi.org/10.1186/1746-4811-7-49
Schmidt R, Kunkowska AB, Schippers JH (2016) Role of reactive oxygen species during cell expansion in leaves. Plant Physiol 172(4):2098–2106. https://doi.org/10.1104/pp.16.00426
Shankar R, Bhattacharjee A, Jain M (2016) Transcriptome analysis in different rice cultivars provides novel insights into desiccation and salinity stress responses. Sci Rep 6(1):1–15. https://doi.org/10.1038/srep23719
Sharan A, Soni P, Nongpiur RC, Singla-Pareek SL, Pareek A (2017) Mapping the “Two-component system” network in rice. Sci Rep 7(1):9287. https://doi.org/10.1038/s41598-017-08076-w
Singh A, Kushwaha HR, Soni P, Gupta H, Singla-Pareek SL, Pareek A (2015) Tissue specific and abiotic stress regulated transcription of histidine kinases in plants is also influenced by diurnal rhythm. Front Plant Sci 6:711. https://doi.org/10.3389/fpls.2015.00711
Sun L, Zhang Q, Wu J et al (2014) Two rice authentic histidine phosphotransfer proteins, OsAHP1 and OsAHP2, mediate cytokinin signaling and stress responses in rice. Plant Physiol 165(1):335–345. https://doi.org/10.1104/pp.113.232629
Takagi H, Tamiru M, Abe A et al (2015) MutMap accelerates breeding of a salt-tolerant rice cultivar. Nat Biotechnol 33(5):445–449. https://doi.org/10.1038/nbt.3188
Tsai YC, Weir NR, Hill K, Zhang W, Kim HJ, Shiu SH, Eric Schaller G, Kieber JJ (2012) Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol 158(4):1666–1684. https://doi.org/10.1104/pp.111.192765
Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143(4):606–616. https://doi.org/10.1016/j.cell.2010.10.020
Urao T, Yamaguchi-Shinozaki K, Shinozaki K (2000) Two-component systems in plant signal transduction. Trends Plant Sci 5(2):67–74. https://doi.org/10.1016/s1360-1385(99)01542-3
Van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433. https://doi.org/10.1146/annurev-arplant-050718
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759. https://doi.org/10.1007/s00726-008-0061-6
Wen F, Qin T, Wang Y, Dong W, Zhang A, Tan M, Jiang M (2015) OsHK3 is a crucial regulator of abscisic acid signaling involved in antioxidant defense in rice. J Integr Plant Biol 57(2):213–228. https://doi.org/10.1111/jipb.12222
Worthen JM, Yamburenko MV, Lim J, Nimchuk ZL, Kieber JJ, Schaller GE (2019) Type-B response regulators of rice play key roles in growth, development and cytokinin signaling. Dev 146(13):dev174870. https://doi.org/10.1242/dev.174870
Yamburenko MV, Worthen JM, Zeenat A, Azhar BJ, Swain S, Couitt AR, Shakeel SN, Kieber JJ, Schaller GE (2020) Functional analysis of the rice type-B response regulator RR22. Front Plant Sci 11:577676. https://doi.org/10.3389/fpls.2020.577676
Yokoyama A, Yamashino T, Amano YI, Tajima Y, Imamura A, Sakakibara H, Mizuno T (2007) Type-B ARR transcription factors, ARR10 and ARR12, are implicated in cytokinin-mediated regulation of protoxylem differentiation in roots of Arabidopsis thaliana. Plant Cell Physiol 48(1):84–96
Zhang A, Liu Y, Wang F et al (2019) Enhanced rice salinity tolerance via CRISPR/Cas9-targeted mutagenesis of the OsRR22 gene. Mol Breed 39:1–10. https://doi.org/10.1007/s11032-019-0954-y
Zhao H, Duan KX, Ma B et al (2020) Histidine kinase MHZ1/OsHK1 interacts with ethylene receptors to regulate root growth in rice. Nat Commun 11(1):518. https://doi.org/10.1038/s41467-020-14313-0
Zubo YO, Schaller GE (2020) Role of the cytokinin-activated type-B response regulators in hormone crosstalk. Plants 9(2):166. https://doi.org/10.3390/plants9020166
Acknowledgements
RCN would like to thank the Council for Scientific and Industrial Research for fellowship. NR acknowledges Department of Biotechnology for providing fellowship.
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RCN and NR performed the experiments. RCN and NR wrote the manuscript. AP and SLSP conceptualized the study and finalized the manuscript. All authors approve the final manuscript.
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Nongpiur, R.C., Rawat, N., Singla-Pareek, S.L. et al. OsRR26, a type-B response regulator, modulates salinity tolerance in rice via phytohormone-mediated ROS accumulation in roots and influencing reproductive development. Planta 259, 96 (2024). https://doi.org/10.1007/s00425-024-04366-6
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DOI: https://doi.org/10.1007/s00425-024-04366-6