Abstract
Rice is an essential but highly stress-susceptible crop, whose root system plays an important role in plant development and stress adaptation. The rice root system architecture is controlled by gene regulatory networks involving different phytohormones including auxin, jasmonate, and gibberellin. Gibberellin is generally known as a molecular clock that interacts with different pathways to regulate root meristem development. The exogenous treatment of rice plantlets with Gibberellin reduced the number of crown roots, whilst the exogenous jasmonic acid treatment enhanced them by involving a Germin-like protein OsGER4. Due to those opposite effects, this study aims to investigate the effect of Gibberellin on crown root development in the rice mutant of the plasmodesmal Germin-like protein OsGER4. Under exogenous gibberellin treatment, the number of crown roots significantly increased in osger4 mutant lines and decreased in the OsGER4 overexpressed lines. GUS staining showed that OsGER4 was strongly expressed in rice root systems, particularly crown and lateral roots under GA3 application. Specifically, OsGER4 was strongly expressed from the exodermis, epidermis, sclerenchyma to the endodermis layers of the crown root, along the vascular bundle and throughout LR primordia. The plasmodesmal protein OsGER4 is suggested to be involved in crown root development by maintaining hormone homeostasis, including Gibberillin.
Data availability
No datasets were generated or analysed during the current study.
References
Amsbury S, Kirk P, Benitez-Alfonso Y (2017) Emerging models on the regulation of intercellular transport by plasmodesmata-associated callose. J Exp Bot 69(1):105–115. https://doi.org/10.1093/JXB/ERX337
Aya K, Tanaka MU, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21(5):1453–1472. https://doi.org/10.1105/TPC.108.062935
Barker R, Fernandez Garcia MN, Powers SJ, Vaughan S, Bennett MJ, Phillips AL, Thomas SG, Hedden P (2021) Mapping sites of gibberellin biosynthesis in the Arabidopsis root tip. New Phytol 229(3):1521–1534. https://doi.org/10.1111/NPH.16967
Bertolotti G, Unterholzner SJ, Scintu D, Salvi E, Svolacchia N, Di Mambro R, Ruta V, Linhares Scaglia F, Vittorioso P, Sabatini S, Costantino P, Dello Ioio R (2021) A PHABULOSA-controlled genetic pathway regulates ground tissue patterning in the Arabidopsis root. Curr Biol 31(2):420-426.e6. https://doi.org/10.1016/J.CUB.2020.10.038
Davière JM, Achard P (2013) Gibberellin signaling in plants. Development (Cambridge, England) 140(6):1147–1151. https://doi.org/10.1242/DEV.087650
E ZG, Ge L, Wang L (2012) Molecular mechanism of adventitious root formation in rice. Plant Growth Regul 68(3):325–331. https://doi.org/10.1007/S10725-012-9721-3/FIGURES/1
Farmer EE, Gasperini D, Acosta IF (2014) The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol 204(2):282–288. https://doi.org/10.1111/NPH.12897
Gallagher SR (1992) Quantitation of GUS activity by fluorometry. In: Gallagher SR (ed) GUS Protocols: using the GUS gene as a reporter of gene expression. Academic Press Inc, New York, pp 47–59
Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17(5):1387–1396. https://doi.org/10.1105/TPC.105.030981
Itoh JI, Nonomura KI, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46(1):23–47. https://doi.org/10.1093/PCP/PCI501
Komatsu S, Konishi H (2005) Proteome analysis of rice root proteins regulated by gibberellin. Genomics Proteomics Bioinformatics 3(3):132–142. https://doi.org/10.1016/S1672-0229(05)03019-6
Kwon CT, Paek NC (2016) Gibberellic acid: a key phytohormone for spikelet fertility in rice grain production. Int J Mol Sci 17(5):794. https://doi.org/10.3390/IJMS17050794
Lakehal A, Bellini C (2019) Control of adventitious root formation: insights into synergistic and antagonistic hormonal interactions. Physiol Plant 165(1):90–100. https://doi.org/10.1111/PPL.12823
Li G, Zhu C, Gan L, Ng D, Xia K (2015) GA(3) enhances root responsiveness to exogenous IAA by modulating auxin transport and signalling in Arabidopsis. Plant Cell Rep 34(3):483–494. https://doi.org/10.1007/S00299-014-1728-Y
Li J, Yang J, Gao Y, Zhang Z, Gao C, Chen S, Liesche J (2024) Parallel auxin transport via PINs and plasmodesmata during the Arabidopsis leaf hyponasty response. Plant Cell Rep 43(1):1–11. https://doi.org/10.1007/S00299-023-03119-1/FIGURES/7
Li J, Yang Y, Chai M, Ren M, Yuan J et al (2020) Gibberellins modulate local auxin biosynthesis and polar auxin transport by negatively affecting flavonoid biosynthesis in the root tips of rice. Plant Sci 298. https://doi.org/10.1016/j.plantsci.2020.110545
Liu S, Wang J, Wang L, Wang X, Xue Y, Wu P, Shou H (2009) Adventitious root formation in rice requires OsGNOM1 and is mediated by the OsPINs family. Cell Res 19(9):1110–1119. https://doi.org/10.1038/cr.2009.70
Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S (2010) The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol 20(12):1138–1143. https://doi.org/10.1016/J.CUB.2010.05.035
Nguyen TT, Pham TD, Do PT et al (2023a) The plasmodesmal protein Osger4 is involved in auxin mediated crown root development in rice. PREPRINT (Version 1) available at Research Square. https://doi.org/10.21203/rs.3.rs-3108300/v1
Nguyen T, Dan Pham T, Tien Do P, Thi Xuan Vo K, Thi Van Le A, Anh Tran T, Ha Chu H, Jeon J-S, Mai Huong To T (2023b) The plasmodesmal protein Osger4 is involved in auxin mediated crown root development in rice. https://doi.org/10.21203/RS.3.RS-3108300/V1
Paquette AJ, Benfey PN (2005) Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiol 138(2):636–640. https://doi.org/10.1104/PP.104.058362
Rinne PLH, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjärvi J, van der Schoot C (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-β-glucanases to reopen signal conduits and release dormancy in populus. Plant Cell 23(1):130–146. https://doi.org/10.1105/TPC.110.081307
Rinne PLH, Paul LK, Vahala J, Kangasjärvi J, Van Der Schoot C (2016) Axillary buds are dwarfed shoots that tightly regulate GA pathway and GA-inducible 1,3-β-glucanase genes during branching in hybrid aspen. J Exp Bot 67(21):5975–5991. https://doi.org/10.1093/JXB/ERW352
Roberts AG, Oparka KJ (2003) Plasmodesmata and the control of symplastic transport. Plant, Cell Environ 26(1):103–124. https://doi.org/10.1046/J.1365-3040.2003.00950.X
Sakata T, Oda S, Tsunaga Y, Shomura H, Kawagishi-Kobayashi M, Aya K, Saeki K, Endo T, Nagano K, Kojima M, Sakakibara H, Watanabe M, Matsuoka M, Higashitani A (2014) Reduction of gibberellin by low temperature disrupts pollen development in rice. Plant Physiol 164(4):2011–2019. https://doi.org/10.1104/PP.113.234401
Shtin M, Dello Ioio R, Del Bianco M (2022) It’s time for a change: the role of gibberellin in root meristem development. Front Plant Sci 13:882517. https://doi.org/10.3389/fpls.2022.882517
Thorpe MR, Ferrieri AP, Herth MM, Ferrieri RA (2007) 11C-imaging: Methyl jasmonate moves in both phloem and xylem, promotes transport of jasmonate, and of photoassimilate even after proton transport is decoupled. Planta 226(2):541–551. https://doi.org/10.1007/S00425-007-0503-5/METRICS
To HTM, Pham DT, Le Thi VA, Nguyen TT, Tran TA, Ta AS, Chu HH, Do PT (2022) The Germin-like protein OsGER4 is involved in promoting crown root development under exogenous jasmonic acid treatment in rice. Plant J 112(3):860–874. https://doi.org/10.1111/TPJ.15987
Ubeda-Tomá S, Federici F, Casimiro I, Beemster GT, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Report gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Current Biology 19:1194–1199. https://doi.org/10.1016/j.cub.2009.06.023
Vlaminck L, Sang-Aram C, Botterman D, Uy CJC, Harper MK, Inzé D, Gheysen G, Depuydt S (2020) Development of a novel and rapid phenotype-based screening method to assess rice seedling growth. Plant Methods 16(1):1–19. https://doi.org/10.1186/S13007-020-00682-6/FIGURES/1
Wang JR, Hu H, Wang GH, Li J, Chen JY, Wu P (2009) Expression of PIN genes in rice (Oryza sativa L.): tissue specificity and regulation by hormones. Mol Plant 2(4):823–831. https://doi.org/10.1093/MP/SSP023
Wang XF, He FF, Ma XX, Mao CZ, Hodgman C, Lu CG, Wu P (2011) OsCAND1 is required for crown root emergence in rice. Mol Plant 4(2):289–299. https://doi.org/10.1093/MP/SSQ068
Wu SW, Kumar R, Iswanto ABB, Kim JY (2018) Callose balancing at plasmodesmata. J Exp Bot 69(22):5325–5339. https://doi.org/10.1093/JXB/ERY317
Zhao H, Ma T, Wang X, Deng Y, Ma H, Zhang R, Zhao J (2015) OsAUX1 controls lateral root initiation in rice (Oryza sativaL.). Plant Cell Environ 38(11):2208–2222. https://doi.org/10.1111/PCE.12467/SUPPINFO
Funding
This work is funded by the Vietnam Academy of Science and Technology under grant number QTKR01.01/24–25.
Author information
Authors and Affiliations
Contributions
TTN, TCN, PTD conducted the experiments. HTMT wrote the manuscript. All authors have read and approved the manuscript for submission.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Nguyen, T.T., Nguyen, T.C., Do, P.T. et al. Effect of gibberellin on crown root development in the mutant of the rice plasmodesmal Germin-like protein OsGER4. Funct Integr Genomics 24, 59 (2024). https://doi.org/10.1007/s10142-024-01341-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10142-024-01341-y