Abstract
Auxin-induced callus formation was largely dependent on the function of Lateral Organ Boundaries Domain (LBD) family transcription factors. We previously revealed that two IGMT (Indole glucosinolate oxy-methyl transferase) genes, IGMT2 and IGMT3, may be involved in the callus formation process as potential target genes of LBD29. Overexpression of the IGMT genes induces spontaneous callus formation. However, the details of the IGMT involvement in callus formation process were not well studied. IGMT1-4, but not IGMT5, are targeted and induced by LBD29 during the early stage of callus formation. Cell membrane and nucleus localized IGMT3 was mainly expressed in the elongation and maturation zones tissues of the primary root and lateral root, which could be further accumulated after CIM treatment. The igmts quadruple mutant, which obtained by CRISPR/Cas9 technology, exhibits a phenotype of attenuated callus formation. Enhanced indole glucosinolate anabolic pathway caused by IGMT1-4 overexpression promotes callus formation. In addition, the IGMT genes were involved in the reactive oxygen species homeostasis, which could be responsible for its role on callus formation. This study provides novel insights into the role of IGMTs gene-mediated callus formation. Activation of the Indole glucosinolate anabolic pathway is an inducing factor for plant callus initiation.
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The data sets generated and analyzed during the current study are available from the corresponding author on reasonable request.
References
Bak S (2001) CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in arabidopsis. Plant Cell 13:101–111. https://doi.org/10.1105/tpc.13.1.101
Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323(5910):101–106. https://doi.org/10.1126/science.1163732
Berckmans B, Vassileva V, Schmid S, Maes S, Parizot B, Naramoto S, Magyar Z, Kamei C, Koncz C, Bögre L, Persiau G, Jaeger GD, Friml J, Simon R, Beeckman T, Veylder LD (2011) Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell 23(10):3671–3683. https://doi.org/10.1105/tpc.111.088377
Castro B, Citterico M, Kimura S, Stevens DM, Wrzaczek M, Coaker G (2021) Stress-induced reactive oxygen species compartmentalization, perception and signalling. Nat Plants 7:403–412. https://doi.org/10.1038/s41477-021-00887-0
Celenza JL (2001) Metabolism of tyrosine and tryptophan-new genes for old pathways. Curr Opin Plant Biol 4(3):234–240. https://doi.org/10.1016/S1369-5266(00)00166-7
Chhajed S, Mostafa I, He Y, Abou-Hashem M, El-Domiaty M, Chen S (2020) Glucosinolate biosynthesis and the glucosinolate–myrosinase system in plant defense. Agronomy 10(11):1786. https://doi.org/10.3390/agronomy10111786
Clay N, Adio A, Denoux C, Jander G, Ausubel F (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323(5910):95–101. https://doi.org/10.1126/science.1164627
Clough SJ, Bent A (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
de Vos M, Kriksunov KL, Jander G (2008) Indole-3-acetonitrile production from indole glucosinolates deters oviposition by Pieris rapae. Plant Physiol 146(3):916–926. https://doi.org/10.1104/pp.107.112185
Dai XH, Liu N, Xiang FN, Liu ZH (2019) MYB94 and MYB96 additively inhibit callus formation via directly repressing LBD29 expression in Arabidopsis thaliana. Plant Sci 293:110323. https://doi.org/10.1016/j.plantsci.2019.110323
Fan J, Crooks C, Creissen G, Hill L, Fairhurst S, Doerner P, Lamb C (2011) Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 331(6021):1185–1188. https://doi.org/10.1126/science.1199707
Fan M, Xu C, Xu K, Hu Y (2012) Lateral organ boundaries domain transcription factors direct callus formation in Arabidopsis regeneration. Cell Res 22(7):1169–1180. https://doi.org/10.1038/cr.2012.63
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of aging. Nature 408(6809):239–247. https://doi.org/10.1038/35041687
Frerigmann H, Gigolashvili T (2014) MYB34, MYB51, and MYB122 distinctly regulate indolic glucosinolate biosynthesis in Arabidopsis thaliana. Mol Plant 7(5):814–828. https://doi.org/10.1093/mp/ssu004
Guan Y, Nothnagel EA (2004) Binding of arabinogalactan proteins by Yariv phenylglycoside triggers wound-like responses in Arabidopsis cell cultures. Plant Physiol 135(3):1346–1366. https://doi.org/10.1104/pp.104.039370
Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333. https://doi.org/10.1146/annurev.arplant.57.032905.105228
Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25(9):3159–3173. https://doi.org/10.1105/tpc.113.116053
Iwase A, Kondo Y, Laohavisit A, Takebayashi A, Ikeuchi M, Matsuoka K, Asahina M, Mitsuda N, Shirasu K, Fukuda H, Sugimoto K (2021) WIND transcription factors orchestrate wound-induced callus formation, vascular reconnection and defense response in Arabidopsis. New Phytol 232:734–752. https://doi.org/10.1111/nph.17594
Jang YL, Sharkis SJ (2007) A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 110(8):3056–3063. https://doi.org/10.1182/blood-2007-05-087759
Ji R, Lei JX, Chen IW, Sang W, Zhu-Salzman K (2020) Cytochrome P450s CYP380C6 and CYP380C9 in green peach aphid facilitate its adaptation to indole glucosinolate-ediated plant defense. Pest Manag Sci 77:148–158. https://doi.org/10.1002/ps.6002
Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49(6):1008–1019. https://doi.org/10.1111/j.1365-313X.2006.03019.x
Lee HW, Kim M-J, Kim NY, Lee SH, Kim J (2012) LBD18 acts as a transcriptional activator that directly binds to the EXPANSIN14 promoter in promoting lateral root emergence of Arabidopsis. Plant J 73:212–224. https://doi.org/10.1111/tpj.12013
Lee HW, Kim NY, Lee DJ, Kim J (2009) LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiol 151:1377–1389. https://doi.org/10.1104/pp.109.143685
Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, Xu L (2014) WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell 26:1081–1093. https://doi.org/10.1105/tpc.114.122887
Ludin A, Gur-Cohen S, Golan K, Kaufmann K, Itkin T, Medaglia C, Lu XJ, Ledergor G, Kollet O, Lapidot T (2014) Reactive oxygen species regulate hematopoietic stem cell self-renewal, migration and development, as well as their bonemarrow microenvironment. Antioxid Redox Sign 21:1605–1619. https://doi.org/10.1089/ars.2014.5941
Mignolet-Spruyt L, Xu EJ, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosche M, Breusegem FV, Kangasjärvi J (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Exp Bot 67(13):3831–3844. https://doi.org/10.1093/jxb/erw080
Mittler R, Zandalinas SI, Fichman Y, Van Breusegem F (2022) Reactive oxygen species signalling in plant stress responses. Nat Rev Mol Cell Biol 23(10):663–679. https://doi.org/10.1038/s41580-022-00499-2
Nagata T, Yamada H, Du Z, Todoriki S, Kikuchi S (2005) Microarray analysis of genes that respond to γ-irradiation in Arabidopsis. J Agric Food Chem 53(4):1022–1030. https://doi.org/10.1021/jf0486895
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130. https://doi.org/10.1105/tpc.106.047761
Pedras MSC, Yaya E, Glawischnig E (2011) ChemInform abstract: the phytoalexins from cultivated and wild crucifers: chemistry and biology. Nat Prod Rep 28:1381–1405. https://doi.org/10.1039/c1np00020a
Pfalz M, Mikkelsen MD, Bednarek P, Olsen CE, Halkier BA, Kroymann J (2011) Metabolic engineering in Nicotiana benthamiana reveals key enzyme functions in Arabidopsis indole glucosinolate modification. Plant Cell 23(2):716–729. https://doi.org/10.1105/tpc.110.081711
Pfalz M, Mukhaimar M, Perreau F, Kirk J, Hansen CIC, Olsen CE, Agerbirk N, Kroymann J (2016) Methyl transfer reactions in glucosinolate biosynthesis mediated by indole glucosinolate O-methyltransferase 5. Plant Physiol 172(4):2190–2203. https://doi.org/10.1104/pp.16.01402
Pfalz M, Vogel H, Kroymann J (2009) The gene controlling the Indole Glucosinolate Modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 21(3):985–999. https://doi.org/10.1105/tpc.108.063115
Porco S, Larrieu A, Du YJ, Gaudinier A, Goh T, Swarup K, Swarup R, Kuempers B, Bishopp A, Lavenus J, Casimiro I, Hill K, Benkova E, Fukaki H, Brady SM, Scheres B, Péret B, Bennett MJ (2016) Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulating auxin influx carrier LAX3. Development 143(18):dev.136283. https://doi.org/10.1242/dev.136283
Reinert J, Backs D (1969) Control of totipotency in plant cells growing in vitro. Nature 220(5174):1340–1341. https://doi.org/10.1038/2201340a0
Rogers L, Dubos C, Cullis I, Surman C, Poole M, Willment J, Mansfield S, Campbell M (2005) Light, the circadian clock, and sugar perception in the control of lignin biosynthesis. J Exp Bot 56(416):1651–1663. https://doi.org/10.1093/jxb/eri162
Shang BS, Xu CY, Zhang XX, Cao HF, Xin W, Hu YX (2016) Very-long-chain fatty acids restrict regeneration capacity by confining pericycle competence for callus formation in Arabidopsis. P Natl Acad Sci USA 113(18):5101–5106. https://doi.org/10.1073/pnas.1522466113
Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11:118–130
Sugimoto K, Gordon SP, Meyerowitz EM (2011) Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol 21(4):212–218. https://doi.org/10.1016/j.tcb.2010.12.004
Sugimoto K, JiaoY L, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18(3):463–471. https://doi.org/10.1016/j.devcel.2010.02.004
Sugiyama M (2018) Partnership for callusing. Nat Plants 4(2):69–70. https://doi.org/10.1038/s41477-018-0104-2
Sun JY, Sonderby IE, Halkier BA, Jander G, de Vos M (2009) Non-volatile intact indole glucosinolates are host recognition cues for ovipositing Plutella xylostella. J Chem Ecol 35(12):1427–1436. https://doi.org/10.1007/s10886-009-9723-4
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197
Tao H, Miao HY, Chen LL, Wang MY, Xia CC, Zeng W, Sun B, Zhang F, Zhang SQ, Li CY (2022) WRKY33-mediated indolic glucosinolate metabolic pathway confers resistance against Alternaria Brassicicola in Arabidopsis and Brassica crops. J Integr Plant Biol 64:1007–1019. https://doi.org/10.1111/jipb.13245
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
Xu CY, Cao HF, Xu EJ, Zhang SQ, Hu YX (2017) Genome-wide identification of Arabidopsis LBD29 target genes reveals the molecular events behind auxin-induced cell reprogramming during callus formation. Plant Cell Physiol 59:749–760. https://doi.org/10.1093/pcp/pcx168
Xu CY, Cao HF, Zhang QQ, Wang HZ, Xin W, Xu EJ, Zhang SQ, Yu RX, Yu DX, Hu YX (2018) Control of auxin-induced callus formation by bZIP59–LBD complex in Arabidopsis regeneration. Nat Plants 4:108–115. https://doi.org/10.1038/s41477-017-0095-4
Xu CY, Hu YX (2020) The molecular regulation of cell pluripotency in plants. Abiotech. https://doi.org/10.1007/s42994-020-00028-9
Xu J, Meng J, Meng XZ, Zhao YT, Liu JM, Sun TF, Liu YD, Wang QM, Zhang SQ (2016) Pathogen-responsive MPK3 and MPK6 reprogram the biosynthesis of indole glucosinolates and their derivatives in Arabidopsis immunity. Plant Cell 28:1144–1162. https://doi.org/10.1105/tpc.15.00871
Yi SY, Lee M, Park SK, Lu L, Lee G, Kim S-G, Kang S-Y, Lim YP (2022) Jasmonate regulates plant resistance to Pectobacterium brasiliense by inducing indole glucosinolate biosynthesis. Front Plant Sci 13:964092. https://doi.org/10.3389/fpls.2022.964092
Yu Y, Xu MM, Ding XH, Chu ZH, Liu HF (2021) Activating the MYB51 and MYB122 to upregulate the transcription of glucosinolates biosynthesis genes by copper ions in Arabidopsis. Plant Physiol Bioch 162:496–505. https://doi.org/10.1016/j.plaphy.2021.03.025
Zeng J, Dong ZC, Wu HJ, Tian ZX, Zhao Z (2017) Redox regulation of plant stem cell fate. EMBO J 36(19):e201695955. https://doi.org/10.15252/embj.201695955
Zhang H, Zhang TT, Liu H, Shi DY, Wang M, Bie XM, Li XG, Zhang XS (2017) Thioredoxin- mediated ros homeostasis explains natural variation in plant regeneration. Plant Physiol 176(3):2231
Zhao YT, Wang JS, Liu YY, Miao HY, Cai CX, Shao ZY, Guo RF, Sun B, Jia CG, Zhang LP, Gigolashvili T, Wang QM (2015) Classic myrosinase-dependent degradation of indole glucosinolate attenuate fumonisin B1-induced programmed cell death in Arabidopsis. Plant J 81:920–933. https://doi.org/10.1111/tpj.12778
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This research was funded by Natural Science Foundation of Shanxi Province (20210302123343), The Program for Scientific and Technological Innovation of Higher Education Institutions in Shanxi (2021L378), Industry-University-Research Project of Shanxi Datong University (2020CXZ16, 2021CXZ6), Shanxi Datong University research project - Yungang study (2021YGZX45), Shanxi Datong University Students Innovation and Entrepreneurship Project (XDC2022147, XDC2022157).
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Cao, H., Zhang, X., Li, F. et al. Glucosinolate O-methyltransferase mediated callus formation and affected ROS homeostasis in Arabidopsis thaliana. Physiol Mol Biol Plants 30, 109–121 (2024). https://doi.org/10.1007/s12298-023-01409-2
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DOI: https://doi.org/10.1007/s12298-023-01409-2