Main conclusion
This study reveals that the process of crown root development and auxin-induced de novo root organogenesis during in vitro plantlet regeneration share a common auxin-OsWOX10 regulatory module in rice.
Abstract
In the fibrous-type root system of rice, the crown roots (CR) are developed naturally from the shoot tissues. Generation of robust auxin response, followed by activation of downstream cell fate determinants and signaling pathways at the onset of crown root primordia (CRP) establishment is essential for new root initiation. During rice tissue culture, embryonic calli are induced to regenerate shoots in vitro which undergo de novo root organogenesis on an exogenous auxin-supplemented medium, but the mechanism underlying spatially restricted root organogenesis remains unknown. Here, we reveal the dynamics of progressive activation of genes involved in auxin homeostasis and signaling during initiation and outgrowth of rice crown root primordia. By comparative global dataset analysis, we identify the crown root primordia-expressed genes whose expression is also regulated by auxin signaling. In-depth spatio-temporal expression pattern analysis shows that the exogenous application of auxin induces a set of key transcription factors exclusively in the spatially positioned CRP. Further, functional analysis of rice WUSCHEL-RELATED HOMEOBOX 10 (OsWOX10) during in vitro plantlet regeneration from embryogenic calli shows that it promotes de novo root organogenesis from regenerated shoots. Expression of rice OsWOX10 also induces adventitious roots (AR) in Arabidopsis, independent of homologous endogenous Arabidopsis genes. Together, our findings reveal that a common auxin-transcription factor regulatory module is involved in root organogenesis under different conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
All data generated or analyzed during this study are provided in this published article and its supplementary data files.
Abbreviations
- AR:
-
Adventitious root
- ARF:
-
Auxin response factor
- Aux/IAA:
-
Auxin/indole acetic acid
- CR:
-
Crown roots
- CRP:
-
Crown root primordia
- LR:
-
Lateral root
- RIM:
-
Root induction media
- SIM:
-
Shoot inducing media
- TF:
-
Transcription factor
References
Atta R, Laurens L, Boucheron-Dubuisson E, Guivarch A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57(4):626–644. https://doi.org/10.1111/j.1365-313X.2008.03715.x
Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65(1):639–666. https://doi.org/10.1146/annurev-arplant-050213-035645
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115(5):591–602. https://doi.org/10.1016/S0092-8674(03)00924-3
Coudert Y, Perin C, Courtois B, Khong NG, Gantet P (2010) Genetic control of root development in rice, the model cereal. Trends Plant Sci 15(4):219–226. https://doi.org/10.1016/j.tplants.2010.01.008
Coudert Y, Le VAT, Adam H, Bès M, Vignols F, Jouannic S, Guiderdoni E, Gantet P (2015) Identification of CROWN ROOTLESS1-regulated genes in rice reveals specific and conserved elements of postembryonic root formation. New Phytol 206(1):243–254. https://doi.org/10.1111/nph.13196
Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S (2008) Activation of the indole-3-acetic acid–amido synthetase GH3-8 suppresses expansin expression and promotes salicylate-and jasmonate-independent basal immunity in rice. Plant Cell 20(1):228–240. https://doi.org/10.1105/tpc.107.055657
Du Y, Scheres B (2017) PLETHORA transcription factors orchestrate de novo organ patterning during Arabidopsis lateral root outgrowth. Proc Natl Acad Sci USA 114(44):11709–11714. https://doi.org/10.1073/pnas.1714410114
Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105(25):8790–8794. https://doi.org/10.1073/pnas.0712307105
Garg T, Singh Z, Chennakesavulu K, Mushahary KKK, Dwivedi AK, Varapparambathu V, Singh H, Singh RS, Sircar D, Chandran D, Prasad K, Jain M, Yadav SR (2022) Species-specific function of conserved regulators in orchestrating rice root architecture. Development 149(9):200381. https://doi.org/10.1242/dev.200381
Gonin M, Jeong K, Coudert Y, Lavarenne J, Hoang GT, Bes M, To HT, Thiaw MR, Do TV, Moukouanga D, Guyomarc’h S et al (2022) CROWN ROOTLESS1 binds DNA with a relaxed specificity and activates OsROP and OsbHLH044 genes involved in crown root formation in rice. Plant J 111(2):546–566. https://doi.org/10.1111/tpj.15838
Greene D, Richardson S, Turro E (2017) ontologyX: a suite of R packages for working with ontological data. Bioinformatics 33(7):1104–1106. https://doi.org/10.1093/bioinformatics/btw763
Guan L, Murphy AS, Peer WA, Gan L, Li Y, Cheng Z-M (2015) Physiological and molecular regulation of adventitious root formation. Crit Rev Plant Sci 34(5):506–521. https://doi.org/10.1080/07352689.2015.1090831
Hu X, Xu L (2016) Transcription factors WOX11/12 directly activate WOX5/7 to promote root primordia initiation and organogenesis. Plant Physiol 172(4):2363–2373. https://doi.org/10.1104/pp.16.01067
Hu Y, Li S, Fan X, Song S, Zhou X, Weng X, Xiao J, Li X, Xiong L, You A, Xing Y (2020) OsHOX1 and OsHOX28 redundantly shape rice tiller angle by reducing HSFA2D expression and auxin content. Plant Physiol 184(3):1424–1437. https://doi.org/10.1104/pp.20.00536
Inukai Y, Miwa M, Nagato Y, Kitano H, Yamauchi A (2001) Characterization of rice mutants deficient in the formation of crown roots. Breed Sci 51(2):123–129. https://doi.org/10.1270/jsbbs.51.123
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 J, Nonomura K, 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
Jing T, Ardiansyah R, Xu Q, Xing Q, Müller-Xing R (2020) Reprogramming of cell fate during root regeneration by transcriptional and epigenetic networks. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00317
Kareem A, Durgaprasad K, Sugimoto K, Du Y, Pulianmackal AJ, Trivedi ZB, Abhayadev PV, Pinon V, Meyerowitz EM, Scheres B, Prasad K (2015) PLETHORA genes control regeneration by a two-step mechanism. Curr Biol 25(8):1017–1030
Kawai T, Shibata K, Akahoshi R, Nishiuchi S, Takahashi H, Nakazono M, Kojima T, Nosaka-Takahashi M, Sato Y, Toyoda A, Lucob-Agustin N (2022) WUSCHEL-related homeobox family genes in rice control lateral root primordium size. Proc Natl Acad Sci USA 119(1):e2101846119. https://doi.org/10.1073/pnas.2101846119
Kidwai M, Mishra P, Bellini C (2023) Species-specific transcriptional reprogramming during adventitious root initiation. Trends Plant Sci 28(2):128–130. https://doi.org/10.1016/j.tplants.2022.11.003
Kitomi Y, Ogawa A, Kitano H, Inukai Y (2008) CRL4 regulates crown root formation through auxin transport in rice. Plant Root 2:19–28. https://doi.org/10.3117/plantroot.2.19
Kitomi Y, Ito H, Hobo T, Aya K, Kitano H, Inukai Y (2011a) The auxin responsive AP2/ERF transcription factor CROWN ROOTLESS5 is involved in crown root initiation in rice through the induction of OsRR1, a type-A response regulator of cytokinin signaling. Plant J 67(3):472–484. https://doi.org/10.1111/j.1365-313X.2011.04610.x
Kitomi Y, Kitano H, Inukai Y (2011b) Molecular mechanism of crown root initiation and the different mechanisms between crown root and radicle in rice. Plant Signal Behav 6(9):1270–1278. https://doi.org/10.4161/psb.6.9.16787
Lavarenne J, Gonin M, Guyomarc’h S, Rouster J, Champion A, Sallaud C, Laplaze L, Gantet P, Lucas M (2019) Inference of the gene regulatory network acting downstream of CROWN ROOTLESS 1 in rice reveals a regulatory cascade linking genes involved in auxin signaling, crown root initiation, and root meristem specification and maintenance. Plant J 100(5):954–968. https://doi.org/10.1111/tpj.14487
Lavarenne J, Gonin M, Champion A, Javelle M, Adam H, Rouster J, Conejéro G, Lartaud M, Verdeil JL, Laplaze L, Sallaud C, Lucas M, Gantet P (2020) Transcriptome profiling of laser-captured crown root primordia reveals new pathways activated during early stages of crown root formation in rice. PLoS ONE 15(11):e0238736. https://doi.org/10.1371/journal.pone.0238736
Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18(8):450–458. https://doi.org/10.1016/j.tplants.2013.04.006
Li Y, Zhu J, Wu L, Shao Y, Wu Y, Mao C (2019) Functional divergence of PIN1 paralogous genes in rice. Plant Cell Physiol 60:2720–2732. https://doi.org/10.1093/pcp/pcz159
Lian G, Ding Z, Wang Q, Zhang D, Xu J (2014) Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom. Sci World J. https://doi.org/10.1155/2014/534140
Liu H, Wang S, Yu X, Yu J, He X, Zhang S, Shou H, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43(1):47–56. https://doi.org/10.1111/j.1365-313X.2005.02434.x
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
Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, Xu L (2014) WOX11 and WOX12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell 26(3):1081–1093. https://doi.org/10.1105/tpc.114.122887
Long Y, Yang Y, Pan G, Shen Y (2022) New insights into tissue culture plant-regeneration mechanisms. Front Plant Sci 13:926752. https://doi.org/10.3389/fpls.2022.926752
Meng F, Xiang D, Zhu J, Li Y, Mao C (2019) Molecular mechanisms of root development in rice. Rice 12:1. https://doi.org/10.1186/s12284-018-0262-x
Motte H, Beeckman T (2019) The evolution of root branching: increasing the level of plasticity. J Exp Bot 70(3):785–793. https://doi.org/10.1093/jxb/ery409
Neogy A, Garg T, Kumar A, Dwivedi AK, Singh H, Singh U, Singh Z, Prasad K, Jain M, Yadav SR (2019) Genome-wide transcript profiling reveals an auxin-responsive transcription factor, OsAP2/ERF-40, promoting rice adventitious root development. Plant Cell Physiol 60(10):2343–2355. https://doi.org/10.1093/pcp/pcz132
Neogy A, Singh Z, Mushahary KK, Yadav SR (2021) Dynamic cytokinin signaling and function of auxin in cytokinin responsive domains during rice crown root development. Plant Cell Rep 40:1367–1375. https://doi.org/10.1007/s00299-020-02618-9
Omary M, Gil-Yarom N, Yahav C, Steiner E, Hendelman A, Efroni I (2022) A conserved superlocus regulates above-and belowground root initiation. Science 375(6584):4368. https://doi.org/10.1126/science.abf4368
Orman-Ligeza B, Parizot B, Gantet P, Beeckman T, Bennett MJ, Draye X (2013) Post-embryonic root organogenesis in cereals: branching out from model plants. Trends Plant Sci 18(8):459–467. https://doi.org/10.1016/j.tplants.2013.04.010
Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14(7):399–408. https://doi.org/10.1016/j.tplants.2009.05.002
Rebouillat J, Dievart A, Verdeil JL, Escoute J, Giese G, Breitler JC, Gantet P, Espeout S, Guiderdoni E, Périn C (2009) Molecular genetics of rice root development. Rice 2:15–34. https://doi.org/10.1007/s12284-008-9016-5
Scarpella E, Rueb S, Boot KJ, Hoge JH, Meijer AH (2000) A role for the rice homeobox gene Oshox1 in provascular cell fate commitment. Development 127(17):3655–3669. https://doi.org/10.1242/dev.127.17.3655
Scarpella E, Rueb S, Meijer AH (2003) The RADICLELESS1 gene is required for vascular pattern formation in rice. Development 130(4):645–658. https://doi.org/10.1242/dev.00243
Shao Y, Zhou HZ, Wu Y, Zhang H, Lin J, Jiang X, He Q, Zhu J, Li Y, Yu H, Mao C (2019) OsSPL3, an SBP-domain protein, regulates crown root development in rice. Plant Cell 31(6):1257–1275. https://doi.org/10.1105/tpc.19.00038
Siligato R, Wang X, Yadav SR, Lehesranta S, Ma G, Ursache R, Sevilem I, Zhang J, Gorte M, Prasad K, Wrzaczek M, Heidstra R, Murphy A, Scheres B, Mähönen AP (2016) MultiSite gateway-compatible cell type-specific gene-inducible system for plants. Plant Physiol 170(2):627–641. https://doi.org/10.1104/pp.15.01246
Singh H, Singh Z, Zhu T, Xu X, Waghmode B, Garg T, Yadav S, Sircar D, De Smet I, Yadav SR (2022a) Auxin-responsive (phospho) proteome analysis reveals key biological processes and signaling associated with shoot-borne crown root development in rice. Plant Cell Physiol 63(12):1968–1979. https://doi.org/10.1093/pcp/pcab155
Singh Z, Singh H, Garg T, Mushahary KK, Yadav SR (2022b) Genetic and hormonal blueprint of shoot-borne adventitious root development in rice and maize. Plant Cell Physiol 63(12):1806–1813. https://doi.org/10.1093/pcp/pcac084
Singh H, Singh Z, Kashyap R, Yadav SR (2023) Lateral root branching: evolutionary innovations and mechanistic divergence in land plants. New Phytol 238(4):1379–1385. https://doi.org/10.1111/nph.18864
Tiwari SB, Wang XJ, Hagen G, Guilfoyle TJ (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13(12):2809–2822. https://doi.org/10.1105/tpc.010289
Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47(6):969–976. https://doi.org/10.1111/j.1365-313X.2006.02836.x
Wang Y, Wang D, Gan T, Liu L, Long W, Wang Y, Niu M, Li X, Zheng M, Jiang L, Wan J (2016) CRL6, a member of the CHD protein family, is required for crown root development in rice. Plant Physiol Biochem 105:185–194. https://doi.org/10.1016/j.plaphy.2016.04.022
Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, Feng T, Zhou L, Tang W, Zhan L, Fu X (2021) clusterProfiler 4.0: A universal enrichment tool for interpreting omics data. The Innovation 2(3):100141. https://doi.org/10.1016/j.xinn.2021.100141
Yadav SR, Khanday I, Majhi BB, Veluthambi K, Vijayraghavan U (2011) Auxin-responsive OsMGH3, a common downstream target of OsMADS1 and OsMADS6, controls rice floret fertility. Plant Cell Physiol 52(12):2123–2135. https://doi.org/10.1093/pcp/pcr142
Yamamoto Y, Kamiya N, Morinaka Y, Matsuoka M, Sazuka T (2007) Auxin biosynthesis by the YUCCA genes in rice. Plant Physiol 143(3):1362–1371. https://doi.org/10.1104/pp.106.091561
Yu J, Liu W, Liu J, Qin P, Xu L (2017) Auxin control of root organogenesis from callus in tissue culture. Front Plant Sci 8(8):1385. https://doi.org/10.3389/fpls.2017.01385
Zhang N, Yu H, Yu H, Cai Y, Huang L, Xu C, Xiong G, Meng X, Wang J, Chen H, Liu G, Jing Y, Yuan Y, Liang Y, Li S, Smith SM, Li J, Wang Y (2018a) A core regulatory pathway controlling rice tiller angle mediated by the LAZY1-dependent asymmetric distribution of auxin. Plant Cell 30(7):1461–1475. https://doi.org/10.1105/tpc.18.00063
Zhang T, Li R, Xing J, Yan L, Wang R, Zhao Y (2018b) The YUCCA-Auxin-WOX11 module controls crown root development in rice. Front Plant Sci 9:523. https://doi.org/10.3389/fpls.2018.00523
Zhao Y, Hu Y, Dai M, Huang L, Zhou DX (2009) The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell 21(3):736–748. https://doi.org/10.1105/tpc.108.061655
Zhao Y, Cheng S, Song Y, Huang Y, Zhou S, Liu X, Zhou DX (2015) The interaction between rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling. Plant Cell 27(9):2469–2483. https://doi.org/10.1105/tpc.15.00227
Acknowledgements
Financial support by the Department of Biotechnology (DBT), Government of India to SRY laboratory (grant# BT/PR13488/BPA/118/105/2015) and to SRY and MJ labs under the National Network Project scheme (grant# BT/PR40261/BTIS/137/55/2023) is acknowledged. The Science and Engineering Research Board (SERB) is acknowledged to provide financing support to SRY (grant# ECR/2016/000060) and MJ (grant# CRG/2020/000172). Indian Institute of Technology, Roorkee (IIT Roorkee) is acknowledged to provide fellowships to TG and KKKM. Fellowships to AK from the Council of Scientific and Industrial Research (CSIR), India, to VP and HS from the University Grant Commission (UGC), India and to MY from the Department of Biotechnology (DBT), India, are gratefully acknowledged. Dr. Lin Xu, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China is acknowledged for kindly providing Arabidopsis wox11-2, wox12-1 and wox11-2 wox12-1 seeds. The destination vector used for Arabidopsis transformation was a gift from Dr. Ari Pekka Mähönen’s lab at the University of Helsinki, Finland. Dr. Leena Yadav is acknowledged for providing critical comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Garg, T., Yadav, M., Mushahary, K.K.K. et al. Spatially activated conserved auxin-transcription factor regulatory module controls de novo root organogenesis in rice. Planta 258, 52 (2023). https://doi.org/10.1007/s00425-023-04210-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04210-3