Advertisement

Science China Life Sciences

, Volume 62, Issue 9, pp 1203–1217 | Cite as

An MAP kinase interacts with LHK1 and regulates nodule organogenesis in Lotus japonicus

  • Jun Yin
  • Xiaomin Guan
  • Heng Zhang
  • Longxiang Wang
  • Hao Li
  • Qing Zhang
  • Tao Chen
  • Zeyuan Xu
  • Zonglie Hong
  • Yangrong CaoEmail author
  • Zhongming ZhangEmail author
Research Paper
  • 142 Downloads

Abstract

Symbiosis receptor-like kinase (SymRK) is a key protein mediating the legume-Rhizobium symbiosis. Our previous work has identified an MAP kinase kinase, SIP2, as a SymRK-interacting protein to positively regulate nodule organogenesis in Lotus japonicus, suggesting that an MAPK cascade might be involved in Rhizobium-legume symbiosis. In this study, LjMPK6 was identified as a phosphorylation target of SIP2. Stable transgenic L. japonicus with RNAi silencing of LjMPK6 decreased the numbers of nodule primordia (NP) and nodule, while plants overexpressing LjMPK6 increased the numbers of nodule, infection threads (ITs), and NP, indicating that LjMPK6 plays a positive role in nodulation. LjMPK6 could interact with a cytokinin receptor, LHK1 both in vivo and in vitro. LjMPK6 was shown to compete with LHP1 to bind to the receiver domain (RD) of LHK1and to downregulate the expression of two LjACS (1-aminocyclopropane-1-carboxylic acid synthase) genes and ethylene levels during nodulation. This study demonstrated an important role of LjMPK6 in regulation of nodule organogenesis and ethylene production in L. japonicus.

Keywords

cytokinin ethylene biosynthesis LHK1 Lotus japonicus MAPK cascade root nodule symbiosis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We thank Dr. K. Szczyglowski (Agriculture and Agri- Food Canada, University of Western Ontario, Canada) for kindly providing LHK1 mutants, Dr. A. Downie (John Innes Centre) for providing M. loti strain R7A carrying pMP2112, Dr. G. Wu (Shanghai Jiao Tong University, China) for providing M. loti MAFF303099, Dr. S. Wang (Huazhong Agricultural University, China) for providing pCAMBIA1301U, L. japonicus LORE1 mutant collection (Centre for Carbohydrate Recongnition and Signaling, Aarhus University, Denmark) for providing LjMPK6 mutants. This work was supported by the National Key R&D Program of China (2016YF0100700), the National Natural Science Foundation of China (31670240 and 31870219), the State Key Laboratory of Agricultural Microbiology (AMLKF201503 and AMLKF201608), the Graduate Education Innovation Fund of Huazhong Agricultural University (to Z.Z.), and Graduate Student Research Innovation Project of Huazhong Agricultural University (to J.Y.).

Compliance and ethics The author(s) declare that they have no conflict of interest.

Supplementary material

11427_2018_9444_MOESM1_ESM.jpg (68 kb)
Figure S1 Expression levels of NIN in L. japonicus.
11427_2018_9444_MOESM2_ESM.jpg (77 kb)
Figure S2 GUS activity analysis in stable transgenic L. japonicus plants expressing LjMPK6pro:GUS.
11427_2018_9444_MOESM3_ESM.jpg (89 kb)
Figure S3 Characterization of an LjMPK6 LORE1 mutant.
11427_2018_9444_MOESM4_ESM.jpg (82 kb)
Figure S4 Gus staining in transgenic plants expressing GUS reporter under the control of LjNAD1 promoter or maize ubiquitin promoter.
11427_2018_9444_MOESM5_ESM.jpg (101 kb)
Figure S5 Infection events in LjMPK6 RNAi and LjMPK6-ox plants.
11427_2018_9444_MOESM6_ESM.jpg (95 kb)
Figure S6 Expression of LjMPK6 in LjMPK6-ox stable transgenic plants under the control of L. japonicus ubiquitin promoter.
11427_2018_9444_MOESM7_ESM.jpg (114 kb)
Figure S7 Immunoblot analysis of protein expression in yeast cells.
11427_2018_9444_MOESM8_ESM.jpg (76 kb)
Figure S8 Competition of BSA with LHP1 for binding to LHK1.
11427_2018_9444_MOESM9_ESM.jpg (56 kb)
Figure S9 Expression of NIN and NSP2 in LjMPK6-ox and LjMPK6-RNAi transgenic plants during nodulation.
11427_2018_9444_MOESM10_ESM.pdf (611 kb)
Supplementary material, approximately 610 KB.
11427_2018_9444_MOESM11_ESM.pdf (21 kb)
Table S1 Primers used in this study
11427_2018_9444_MOESM12_ESM.pdf (14 kb)
Table S2 Accession numbers of genes used in this study

References

  1. Berriri, S., Garcia, A.V., Frei dit Frey, N., Rozhon, W., Pateyron, S., Leonhardt, N., Montillet, J.L., Leung, J., Hirt, H., and Colcombet, J. (2012). Constitutively active mitogen-activated protein kinase versions reveal functions of Arabidopsis MPK4 in pathogen defense signaling. Plant Cell 24, 4281–4293.CrossRefGoogle Scholar
  2. Brodersen, P., Petersen, M., Bjørn Nielsen, H., Zhu, S., Newman, M.A., Shokat, K.M., Rietz, S., Parker, J., and Mundy, J. (2006). Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J 47, 532–546.CrossRefGoogle Scholar
  3. Cao, Y., Halane, M.K., Gassmann, W., and Stacey, G. (2017). The role of plant innate immunity in the legume-rhizobium symbiosis. Annu Rev Plant Biol 68, 535–561.CrossRefGoogle Scholar
  4. Cardinale, F., Meskiene, I., Ouaked, F., and Hirt, H. (2002). Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases. Plant Cell 14, 703–711.Google Scholar
  5. Chae, H.S., and Kieber, J.J. (2005). Eto Brute? Role of ACS turnover in regulating ethylene biosynthesis. Trends Plant Sci 10, 291–296.CrossRefGoogle Scholar
  6. Chai, J., Liu, J., Zhou, J., and Xing, D. (2014). Mitogen-activated protein kinase 6 regulates NPR1 gene expression and activation during leaf senescence induced by salicylic acid. J Exp Bot 65, 6513–6528.CrossRefGoogle Scholar
  7. Chen, T., Zhou, B., Duan, L., Zhu, H., and Zhang, Z. (2017). MtMAPKK4 is an essential gene for growth and reproduction of Medicago truncatula. Physiol Plantarum 159, 492–503.CrossRefGoogle Scholar
  8. Chen, T., Zhu, H., Ke, D., Cai, K., Wang, C., Gou, H., Hong, Z., and Zhang, Z. (2012). A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus japonicus. Plant Cell 24, 823–838.CrossRefGoogle Scholar
  9. de Zelicourt, A., Colcombet, J., and Hirt, H. (2016). The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21, 677–685.CrossRefGoogle Scholar
  10. Dortay, H., Mehnert, N., Bürkle, L., Schmülling, T., and Heyl, A. (2006). Analysis of protein interactions within the cytokinin-signaling pathway of Arabidopsis thaliana. FEBS J 273, 4631–4644.CrossRefGoogle Scholar
  11. Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kaló, P., and Kiss, G.B. (2002). A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966.CrossRefGoogle Scholar
  12. Frankowski, K., Kesy, J., and Kopcewicz, J. (2007). Regulation of ethylene biosynthesis in plants. Postepy Biochem 53, 66–73.Google Scholar
  13. Fukai, E., Soyano, T., Umehara, Y., Nakayama, S., Hirakawa, H., Tabata, S., Sato, S., and Hayashi, M. (2012). Establishment of a Lotus japonicus gene tagging population using the exon-targeting endogenous retrotransposon LORE1. Plant J 69, 720–730.CrossRefGoogle Scholar
  14. Gamas, P., Brault, M., Jardinaud, M.F., and Frugier, F. (2017). Cytokinins in symbiotic nodulation: when, where, what for? Trends Plant Sci 22, 792–802.CrossRefGoogle Scholar
  15. Gao, M., Liu, J., Bi, D., Zhang, Z., Cheng, F., Chen, S., and Zhang, Y. (2008). MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 18, 1190–1198.CrossRefGoogle Scholar
  16. Gonzalez-Rizzo, S., Crespi, M., and Frugier, F. (2006). The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18, 2680–2693.CrossRefGoogle Scholar
  17. Gresshoff, P.M. (2003). Post-genomic insights into plant nodulation symbioses. Genome Biol 4, 201.CrossRefGoogle Scholar
  18. Gudesblat, G.E., Iusem, N.D., and Morris, P.C. (2007). Arabidopsis MPK3, a key signalling intermediate in stomatal function. Plant Signal Behav 2, 271–272.CrossRefGoogle Scholar
  19. Han, L., Li, G.J., Yang, K.Y., Mao, G., Wang, R., Liu, Y., and Zhang, S. (2010). Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. Plant J 48, no.Google Scholar
  20. Hansen, M., Chae, H.S., and Kieber, J.J. (2009). Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J 57, 606–614.CrossRefGoogle Scholar
  21. Heidstra, R., Geurts, R., Franssen, H., Spaink, H.P., van Kammen, A., and Bisseling, T. (1994). Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol 105, 787–797.CrossRefGoogle Scholar
  22. Held, M., Hou, H., Miri, M., Huynh, C., Ross, L., Hossain, M.S., Sato, S., Tabata, S., Perry, J., Wang, T.L., et al. (2014). Lotus japonicus cytokinin receptors work partially redundantly to mediate nodule formation. Plant Cell 26, 678–694.CrossRefGoogle Scholar
  23. Hettenhausen, C., Schuman, M.C., and Wu, J. (2015). MAPK signaling: A key element in plant defense response to insects. Insect Sci 22, 157–164.CrossRefGoogle Scholar
  24. Hutchison, C.E., and Kieber, J.J. (2002). Cytokinin signaling in Arabidopsis. Plant Cell 14, S47–S59.CrossRefGoogle Scholar
  25. Hwang, I., and Sheen, J. (2001). Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383–389.CrossRefGoogle Scholar
  26. Jia, W., Li, B., Li, S., Liang, Y., Wu, X., Ma, M., Wang, J., Gao, J., Cai, Y., Zhang, Y., et al. (2016). Mitogen-activated protein kinase cascade MKK7-MPK6 plays important roles in plant development and regulates shoot branching by phosphorylating PIN1 in Arabidopsis. PLoS Biol 14, e1002550.CrossRefGoogle Scholar
  27. Joo, S., Liu, Y., Lueth, A., and Zhang, S. (2008). MAPK phosphorylationinduced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. Plant J 54, 129–140.CrossRefGoogle Scholar
  28. Kiegerl, S., Cardinale, F., Siligan, C., Gross, A., Baudouin, E., Liwosz, A., Eklöf, S., Till, S., Bögre, L., Hirt, H., et al. (2000). SIMKK, a mitogenactivated protein kinase (MAPK) kinase, is a specific activator of the salt stress-induced MAPK, SIMK. Plant Cell 12, 2247–2258.Google Scholar
  29. Kim, C.Y., Liu, Y., Thorne, E.T., Yang, H., Fukushige, H., Gassmann, W., Hildebrand, D., Sharp, R.E., and Zhang, S. (2003). Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 15, 2707–2718.CrossRefGoogle Scholar
  30. Li, G., Meng, X., Wang, R., Mao, G., Han, L., Liu, Y., and Zhang, S. (2012). Dual-level regulation of ACC synthase activity by MPK3/ MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet 8, e1002767.CrossRefGoogle Scholar
  31. Liu, J.Z., Braun, E., Qiu, W.L., Shi, Y.F., Marcelino-Guimarães, F.C., Navarre, D., Hill, J.H., and Whitham, S.A. (2014). Positive and negative roles for soybean MPK6 in regulating defense responses. MPMI 27, 824–834.CrossRefGoogle Scholar
  32. Liu, Y., and Zhang, S. (2004). Phosphorylation of 1-aminocyclopropane-1- carboxylic acid synthase by MPK6, a stress-responsive mitogenactivated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16, 3386–3399.CrossRefGoogle Scholar
  33. Lopez-Gomez, M., Sandal, N., Stougaard, J., and Boller, T. (2012). Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J Exp Bot 63, 393–401.CrossRefGoogle Scholar
  34. Lu, C., Han, M.H., Guevara-Garcia, A., and Fedoroff, N.V. (2002). Nonlinear partial differential equations and applications: Mitogenactivated protein kinase signaling in postgermination arrest of development by abscisic acid. Proc Natl Acad Sci USA 99, 15812–15817.CrossRefGoogle Scholar
  35. Madsen, E.B., Madsen, L.H., Radutoiu, S., Olbryt, M., Rakwalska, M., Szczyglowski, K., Sato, S., Kaneko, T., Tabata, S., Sandal, N., et al. (2003). A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals. Nature 425, 637–640.CrossRefGoogle Scholar
  36. Maekawa, T., Kusakabe, M., Shimoda, Y., Sato, S., Tabata, S., Murooka, Y., and Hayashi, M. (2008). Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. MPMI 21, 375–382.CrossRefGoogle Scholar
  37. Mähönen, A.P., Higuchi, M., Törmäkangas, K., Miyawaki, K., Pischke, M. S., Sussman, M.R., Helariutta, Y., and Kakimoto, T. (2006). Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr Biol 16, 1116–1122.CrossRefGoogle Scholar
  38. Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z., and Zhang, S. (2011). Phosphorylation of a WRKY transcription factor by two pathogenresponsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23, 1639–1653.CrossRefGoogle Scholar
  39. Meldau, S., Ullman-Zeunert, L., Govind, G., Bartram, S., and Baldwin, I.T. (2012). MAPK-dependent JA and SA signalling in Nicotiana attenuata affects plant growth and fitness during competition with conspecifics. BMC Plant Biol 12, 213.CrossRefGoogle Scholar
  40. Meng, X., Xu, J., He, Y., Yang, K.Y., Mordorski, B., Liu, Y., and Zhang, S. (2013). Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 25, 1126–1142.CrossRefGoogle Scholar
  41. Meng, Y., Ma, N., Zhang, Q., You, Q., Li, N., Ali Khan, M., Liu, X., Wu, L., Su, Z., and Gao, J. (2014). Precise spatio-temporal modulation of ACC synthase by MPK6 cascade mediates the response of rose flowers to rehydration. Plant J 79, 941–950.CrossRefGoogle Scholar
  42. Miller, J.B., Pratap, A., Miyahara, A., Zhou, L., Bornemann, S., Morris, R. J., and Oldroyd, G.E.D. (2013). Calcium/Calmodulin-dependent protein kinase is negatively and positively regulated by calcium, providing a mechanism for decoding calcium responses during symbiosis signaling. Plant Cell 25, 5053–5066.CrossRefGoogle Scholar
  43. Minkenberg, B., Xie, K., and Yang, Y. (2017). Discovery of rice essential genes by characterizing a CRISPR-edited mutation of closely related rice MAP kinase genes. Plant J 89, 636–648.CrossRefGoogle Scholar
  44. Miri, M., Janakirama, P., Held, M., Ross, L., and Szczyglowski, K. (2016). Into the root: how cytokinin controls rhizobial infection. Trends Plant Sci 21, 178–186.CrossRefGoogle Scholar
  45. Miyata, K., Kawaguchi, M., and Nakagawa, T. (2013). Two distinct EIN2 genes cooperatively regulate ethylene signaling in Lotus japonicus.. Plant Cell Physiol 54, 1469–1477.CrossRefGoogle Scholar
  46. Morieri, G., Martinez, E.A., Jarynowski, A., Driguez, H., Morris, R., Oldroyd, G.E.D., and Downie, J.A. (2013). Host-specific Nod-factors associated with Medicago truncatula nodule infection differentially induce calcium influx and calcium spiking in root hairs. New Phytol 200, 656–662.CrossRefGoogle Scholar
  47. Mortier, V., Holsters, M., and Goormachtig, S. (2012). Never too many? How legumes control nodule numbers. Plant Cell Environ 35, 245–258.CrossRefGoogle Scholar
  48. Moussatche, P., and Klee, H.J. (2004). Autophosphorylation activity of the Arabidopsis ethylene receptor multigene family. J Biol Chem 279, 48734–48741.CrossRefGoogle Scholar
  49. Murray, J.D., Karas, B.J., Sato, S., Tabata, S., Amyot, L., and Szczyglowski, K. (2007). A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315, 101–104.CrossRefGoogle Scholar
  50. Nakagami, H., Pitzschke, A., and Hirt, H. (2005). Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10, 339–346.CrossRefGoogle Scholar
  51. Neupane, A., Nepal, M.P., Benson, B.V., Macarthur, K.J., and Piya, S. (2013). Evolutionary history of mitogen-activated protein kinase (MAPK) genes in Lotus, Medicago, and Phaseolus. Plant Signal Behav 8, e27189.CrossRefGoogle Scholar
  52. Nie, S., and Xu, H. (2016). Riboflavin-induced disease resistance requires the mitogen-activated protein kinases 3 and 6 in Arabidopsis thaliana. PLoS ONE 11, e0153175.CrossRefGoogle Scholar
  53. Oldroyd, G.E.D., Engstrom, E.M., and Long, S.R. (2001). Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13, 1835–1849.CrossRefGoogle Scholar
  54. Penmetsa, R.V., and Cook, D.R. (1997). A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527–530.CrossRefGoogle Scholar
  55. Pitzschke, A. (2015). Modes of MAPK substrate recognition and control. Trends Plant Sci 20, 49–55.CrossRefGoogle Scholar
  56. Punwani, J.A., Hutchison, C.E., Schaller, G.E., and Kieber, J.J. (2010). The subcellular distribution of the Arabidopsis histidine phosphotransfer proteins is independent of cytokinin signaling. Plant J 62, 473–482.CrossRefGoogle Scholar
  57. Radutoiu, S., Madsen, L.H., Madsen, E.B., Felle, H.H., Umehara, Y., Grønlund, M., Sato, S., Nakamura, Y., Tabata, S., Sandal, N., et al. (2003). Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592.CrossRefGoogle Scholar
  58. Rasmussen, M.W., Roux, M., Petersen, M., and Mundy, J. (2012). MAP kinase cascades in Arabidopsis innate immunity. Front Plant Sci 3, 169.CrossRefGoogle Scholar
  59. Reid, D., Liu, H., Kelly, S., Kawaharada, Y., Mun, T., Andersen, S.U., Desbrosses, G., and Stougaard, J. (2018). Dynamics of ethylene production in response to compatible Nod factor. Plant Physiol 176, 1764–1772.CrossRefGoogle Scholar
  60. Ryu, H., Laffont, C., Frugier, F., and Hwang, I. (2017). MAP kinasemediated negative regulation of symbiotic nodule formation in Medicago truncatula. Mol Cells 40, 17–23.CrossRefGoogle Scholar
  61. Sasaki, T., Suzaki, T., Soyano, T., Kojima, M., Sakakibara, H., and Kawaguchi, M. (2014). Shoot-derived cytokinins systemically regulate root nodulation. Nat Commun 5, 4983.CrossRefGoogle Scholar
  62. Schauser, L., Handberg, K., Sandal, N., Stiller, J., Thykjaer, T., Pajuelo, E., Nielsen, A., and Stougaard, J. (1998). Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus. Mol Gen Genet 259, 414–423.CrossRefGoogle Scholar
  63. Singh, P., Mohanta, T.K., and Sinha, A.K. (2015). Unraveling the intricate nexus of molecular mechanisms governing rice root development: OsMPK3/6 and auxin-cytokinin interplay. PLoS ONE 10, e0123620.CrossRefGoogle Scholar
  64. Stanko, V., Giuliani, C., Retzer, K., Djamei, A., Wahl, V., Wurzinger, B., Wilson, C., Heberle-Bors, E., Teige, M., and Kragler, F. (2015). Timing is everything: highly specific and transient expression of a MAP kinase determines auxin-induced leaf venation patterns in Arabidopsis. Mol Plant 8, 829.CrossRefGoogle Scholar
  65. Takahashi, F., Yoshida, R., Ichimura, K., Mizoguchi, T., Seo, S., Yonezawa, M., Maruyama, K., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2007). The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 19, 805–818.CrossRefGoogle Scholar
  66. Tanaka, Y., Suzuki, T., Yamashino, T., and Mizuno, T. (2004). Comparative studies of the AHP histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in Arabidopsis thaliana. Biosci Biotech Biochem 68, 462–465.CrossRefGoogle Scholar
  67. Tirichine, L., Sandal, N., Madsen, L.H., Radutoiu, S., Albrektsen, A.S., Sato, S., Asamizu, E., Tabata, S., and Stougaard, J. (2007). A gain-offunction mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315, 104–107.CrossRefGoogle Scholar
  68. Urbanski, D.F., Malolepszy, A., Stougaard, J., and Andersen, S.U. (2012). Genome-wide LORE1 retrotransposon mutagenesis and highthroughput insertion detection in Lotus japonicus. Plant J 69, 731–741.CrossRefGoogle Scholar
  69. van Zeijl, A., Op den Camp, R.H.M., Deinum, E.E., Charnikhova, T., Franssen, H., Op den Camp, H.J.M., Bouwmeester, H., Kohlen, W., Bisseling, T., and Geurts, R. (2015). Rhizobium lipochitooligosaccharide signaling triggers accumulation of cytokinins in Medicago truncatula roots. Mol Plant 8, 1213–1226.CrossRefGoogle Scholar
  70. Verma, V., Sivaraman, J., Srivastava, A.K., Sadanandom, A., and Kumar, P. P. (2015). Destabilization of interaction between cytokinin signaling intermediates AHP1 and ARR4 modulates Arabidopsis development. New Phytol 206, 726–737.CrossRefGoogle Scholar
  71. Vijn, I., Das Neves, L., van Kammen, A., Franssen, H., and Bisseling, T. (1993). Nod factors and nodulation in plants. Science 260, 1764–1765.CrossRefGoogle Scholar
  72. Wang, C., Yu, H., Luo, L., Duan, L., Cai, L., He, X., Wen, J., Mysore, K.S., Li, G., Xiao, A., et al. (2016). NODULES WITH ACTIVATED DEFENSE 1 is required for maintenance of rhizobial endosymbiosis in Medicago truncatula. New Phytol 212, 176–191.CrossRefGoogle Scholar
  73. Wang, C., Zhu, M., Duan, L., Yu, H., Chang, X., Li, L., Kang, H., Feng, Y., Zhu, H., Hong, Z., et al. (2015). Lotus japonicus clathrin heavy Chain1 is associated with Rho-like GTPase ROP6 and involved in nodule formation. Plant Physiol 167, 1497–1510.CrossRefGoogle Scholar
  74. Wang, H., Ngwenyama, N., Liu, Y., Walker, J.C., and Zhang, S. (2007). Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19, 63–73.CrossRefGoogle Scholar
  75. Wang, P., and Zhu, J.K. (2016). Assessing kinase activity in plants with ingel kinase assays. Methods Mol Biol 1363, 189–197.CrossRefGoogle Scholar
  76. Wopereis, J., Pajuelo, E., Dazzo, F.B., Jiang, Q., Gresshoff, P.M., de Bruijn, F.J., Stougaard, J., and Szczyglowski, K. (2000). Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J 23, 97–114.CrossRefGoogle Scholar
  77. Xu, J., Meng, J., Meng, X., Zhao, Y., Liu, J., Sun, T., Liu, Y., Wang, Q., and Zhang, S. (2016). Pathogen-responsive MPK3 and MPK6 reprogram the biosynthesis of indole glucosinolates and their derivatives in Arabidopsis immunity. Plant Cell 28, 1144–1162.CrossRefGoogle Scholar
  78. Xu, J., and Zhang, S. (2015). Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci 20, 56–64.CrossRefGoogle Scholar
  79. Yi, J., Lee, Y.S., Lee, D.Y., Cho, M.H., Jeon, J.S., and An, G. (2016). OsMPK6 plays a critical role in cell differentiation during early embryogenesis in Oryza sativa. J Exp Bot 67, 2425–2437.CrossRefGoogle Scholar
  80. Zhou, C., Cai, Z., Guo, Y., and Gan, S. (2009). An Arabidopsis mitogenactivated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol 150, 167–177.CrossRefGoogle Scholar
  81. Zhu, H., Chen, T., Zhu, M., Fang, Q., Kang, H., Hong, Z., and Zhang, Z. (2008). A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus. Plant Physiol 148, 337–347.CrossRefGoogle Scholar
  82. Zong, W., Tang, N., Yang, J., Peng, L., Ma, S., Xu, Y., Li, G., and Xiong, L. (2016). Feedback regulation of ABA signaling and biosynthesis by a bZIP transcription factor targets drought resistance related genes. Plant Physiol 171, 2810–2825.Google Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Jun Yin
    • 1
  • Xiaomin Guan
    • 1
  • Heng Zhang
    • 1
  • Longxiang Wang
    • 1
  • Hao Li
    • 1
  • Qing Zhang
    • 1
  • Tao Chen
    • 1
  • Zeyuan Xu
    • 1
  • Zonglie Hong
    • 2
  • Yangrong Cao
    • 1
    Email author
  • Zhongming Zhang
    • 1
    Email author
  1. 1.State Key Laboratory of Agricultural Microbiology, College of Life Science and TechnologyHuazhong Agricultural UniversityWuhanChina
  2. 2.Department of Plant, Soil and Entomological Sciences and Program of Microbiology, Molecular Biology and BiochemistryUniversity of IdahoMoscowUSA

Personalised recommendations