The role of Class Ⅱ KNOX family in controlling compound leaf patterning in Medicago truncatula.


Journal

Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502

Informations de publication

Date de publication:
Oct 2023
Historique:
received: 04 04 2023
accepted: 31 07 2023
medline: 27 10 2023
pubmed: 1 8 2023
entrez: 1 8 2023
Statut: ppublish

Résumé

Compound leaf development requires the coordination of genetic factors, hormones, and other signals. In this study, we explored the functions of Class Ⅱ KNOTTED-like homeobox (KNOXII) genes in the model leguminous plant Medicago truncatula. Phenotypic and genetic analyses suggest that MtKNOX4, 5 are able to repress leaflet formation, while MtKNOX3, 9, 10 are not involved in this developmental process. Further investigations have shown that MtKNOX4 represses the CK signal transduction, which is downstream of MtKNOXⅠ-mediated CK biosynthesis. Additionally, two boundary genes, FUSED COMPOUND LEAF1 (orthologue of Arabidopsis Class M KNOX) and NO APICAL MERISTEM (orthologue of Arabidopsis CUP-SHAPED COTYLEDON), are necessary for MtKNOX4-mediated compound leaf formation. These findings suggest, that among the members of MtKNOXⅡ, MtKNOX4 plays a crucial role in integrating the CK pathway and boundary regulators, providing new insights into the roles of MtKNOXⅡ in regulating the elaboration of compound leaves in M. truncatula.

Identifiants

pubmed: 37526388
doi: 10.1111/jipb.13549
doi:

Substances chimiques

Plant Proteins 0
Homeodomain Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2279-2291

Subventions

Organisme : National Natural Science Foundation of China
ID : 31972958
Organisme : National Natural Science Foundation of China
ID : 32100284
Organisme : National Natural Science Foundation of China
ID : 32170833
Organisme : National Natural Science Foundation of Shandong Province
ID : ZR2020KC018
Organisme : National Natural Science Foundation of Shandong Province
ID : ZR202103010073

Informations de copyright

© 2023 Institute of Botany, Chinese Academy of Sciences.

Références

Andriankaja, M., Dhondt, S., De Bodt, S., Vanhaeren, H., Coppens, F., De Milde, L., Muhlenbock, P., Skirycz, A., Gonzalez, N., Beemster, G.T., et al. (2012). Exit from proliferation during leaf development in Arabidopsis thaliana: A not-so-gradual process. Dev. Cell 22: 64-78.
Azarakhsh, M., Kirienko, A.N., Zhukov, V.A., Lebedeva, M.A., Dolgikh, E.A., and Lutova, L.A. (2015). KNOTTED1-LIKE HOMEOBOX 3: a new regulator of symbiotic nodule development. J. Exp. Bot. 66: 7181-7195.
Azarakhsh, M., Rumyantsev, A.M., Lebedeva, M.A., and Lutova, L.A. (2020). Cytokinin biosynthesis genes expressed during nodule organogenesis are directly regulated by the KNOX3 protein in Medicago truncatula. PLoS ONE 15: e0232352.
Bar, M., and Ori, N. (2014). Leaf development and morphogenesis. Development 141: 4219-4230.
Barkoulas, M., Galinha, C., Grigg, S.P., and Tsiantis, M. (2007). From genes to shape: Regulatory interactions in leaf development. Curr. Opin. Plant Biol. 10: 660-666.
Ben-Gera, H., Shwartz, I., Shao, M.R., Shani, E., Estelle, M., and Ori, N. (2012). ENTIRE and GOBLET promote leaflet development in tomato by modulating auxin response. Plant J. 70: 903-915.
Berger, Y., Harpaz-Saad, S., Brand, A., Melnik, H., Sirding, N., Alvarez, J.P., Zinder, M., Samach, A., Eshed, Y., and Ori, N. (2009). The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136: 823-832.
Bharathan, G., Goliber, T.E., Moore, C., Kessler, S., Pham, T., and Sinha, N.R. (2002). Homologies in leaf form inferred from KNOXI gene expression during development. Science 296: 1858-1860.
Bhargava, A., Ahad, A., Wang, S., Mansfield, S.D., Haughn, G.W., Douglas, C.J., and Ellis, B.E. (2013). The interacting MYB75 and KNAT7 transcription factors modulate secondary cell wall deposition both in stems and seed coat in Arabidopsis. Planta 237: 1199-1211.
Bhargava, A., Mansfield, S.D., Hall, H.C., Douglas, C.J., and Ellis, B.E. (2010). MYB75 functions in regulation of secondary cell wall formation in the Arabidopsis inflorescence stem. Plant Physiol. 154: 1428-1438.
Blein, T., Pulido, A., Vialette-Guiraud, A., Nikovics, K., Morin, H., Hay, A., Johansen, I.E., Tsiantis, M., and Laufs, P. (2008). A conserved molecular framework for compound leaf development. Science 322: 1835-1839.
Chai, M., Zhou, C., Molina, I., Fu, C., Nakashima, J., Li, G., Zhang, W., Park, J., Tang, Y., Jiang, Q., et al. (2016). A class II KNOX gene, KNOX4, controls seed physical dormancy. Proc. Natl. Acad. Sci. U.S.A. 113: 6997-7002.
Challa, K.R., Rath, M., Sharma, A.N., Bajpai, A.K., Davuluri, S., Acharya, K.K., and Nath, U. (2021). Active suppression of leaflet emergence as a mechanism of simple leaf development. Nat. Plants 7: 1264-1275.
Champagne, C., and Sinha, N. (2004). Compound leaves: Equal to the sum of their parts? Development 131: 4401-4412.
Champagne, C.E., Goliber, T.E., Wojciechowski, M.F., Mei, R.W., Townsley, B.T., Wang, K., Paz, M.M., Geeta, R., and Sinha, N.R. (2007). Compound leaf development and evolution in the legumes. Plant Cell 19: 3369-3378.
Cheng, X., Peng, J., Ma, J., Tang, Y., Chen, R., Mysore, K.S., and Wen, J. (2012). NO APICAL MERISTEM (MtNAM) regulates floral organ identity and lateral organ separation in Medicago truncatula. New Phytol. 195: 71-84.
Cheng, X., Wang, M., Lee, H.K., Tadege, M., Ratet, P., Udvardi, M., Mysore, K.S., and Wen, J. (2014). An efficient reverse genetics platform in the model legume Medicago truncatula. New Phytol. 201: 1065-1076.
Conklin, P.A., Strable, J., Li, S., and Scanlon, M.J. (2018). On the mechanisms of development in monocot and eudicot leaves. New Phytol. 221: 706-724.
Das Gupta, M., and Tsiantis, M. (2018). Gene networks and the evolution of plant morphology. Curr. Opin. Plant Biol. 45: 82-87.
Di Giacomo, E., Laffont, C., Sciarra, F., Iannelli, M.A., Frugier, F., and Frugis, G. (2016). KNAT3/4/5-like class 2 KNOX transcription factors are involved in Medicago truncatula symbiotic nodule organ development. New Phytol. 213: 822-837.
Di Giacomo, E., Sestili, F., Iannelli, M.A., Testone, G., Mariotti, D., and Frugis, G. (2008). Characterization of KNOX genes in Medicago truncatula. Plant Mol. Biol. 67: 135-150.
Du, F., Mo, Y., Israeli, A., Wang, Q., Yifhar, T., Ori, N., and Jiao, Y. (2020). Leaflet initiation and blade expansion are separable in compound leaf development. Plant J. 104: 1073-1087.
Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616-629.
Furumizu, C., Alvarez, J.P., Sakakibara, K., and Bowman, J.L. (2015). Antagonistic roles for KNOX1 and KNOX2 genes in patterning the land plant body plan following an ancient gene duplication. PLoS Genet. 11: e1004980.
Gong, S.Y., Huang, G.Q., Sun, X., Qin, L.X., Li, Y., Zhou, L., and Li, X.B. (2014). Cotton KNL1, encoding a class II KNOX transcription factor, is involved in regulation of fibre development. J. Exp. Bot. 65: 4133-4147.
Greenboim-Wainberg, Y., Maymon, I., Borochov, R., Alvarez, J., Olszewski, N., Ori, N., Eshed, Y., and Weiss, D. (2005). Cross talk between gibberellin and cytokinin: The Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 17: 92-102.
Gupta, M.D., and Tsiantis, M. (2018). Gene networks and the evolution of plant morphology. Curr. Opin. Plant Biol. 45: 82-87.
Hareven, D., Gutfinger, T., Parnis, A., Eshed, Y., and Lifschitz, E. (1996). The making of a compound leaf: Genetic manipulation of leaf architecture in tomato. Cell 84: 735-744.
Hay, A., and Tsiantis, M. (2006). The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat. Genet. 38: 942-947.
Hay, A., and Tsiantis, M. (2010). KNOX genes: Versatile regulators of plant development and diversity. Development 137: 3153-3165.
He, J.B., Zhao, X.H., Du, P.Z., Zeng, W., Beahan, C.T., Wang, Y.Q., Li, H.L., Bacic, A., and Wu, A.M. (2018). KNAT7 positively regulates xylan biosynthesis by directly activating IRX9 expression in Arabidopsis. J. Integr. Plant Biol. 60: 514-528.
Ichihashi, Y., and Tsukaya, H. (2015). Behavior of leaf meristems and their modification. Front. Plant Sci. 6: 1060.
Janssen, B.J., Lund, L., and Sinha, N. (1998). Overexpression of a homeobox gene, LeT6, reveals indeterminate features in the tomato compound leaf. Plant Physiol. 117: 771-786.
Jasinski, S., Piazza, P., Craft, J., Hay, A., Woolley, L., Rieu, I., Phillips, A., Hedden, P., and Tsiantis, M. (2005). KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 15: 1560-1565.
Jiao, K., Li, X., Guo, Y., Guan, Y., Guo, W., Luo, D., Hu, Z., and Shen, Z. (2019). Regulation of compound leaf development in mungbean (Vigna radiata L.) by CUP-SHAPED COTYLEDON/NO APICAL MERISTEM (CUC/NAM) gene. Planta 249: 765-774.
Kanrar, S., Onguka, O., and Smith, H.M. (2006). Arabidopsis inflorescence architecture requires the activities of KNOX-BELL homeodomain heterodimers. Planta 224: 1163-1173.
Keren-Keiserman, A., Shtern, A., Levy, M., Chalupowicz, D., Furumizu, C., Alvarez, J.P., Amsalem, Z., Arazi, T., Alkalai-Tuvia, S., Efroni, I., et al. (2022). CLASS-II KNOX genes coordinate spatial and temporal ripening in tomato. Plant Physiol. 190: 657-668.
Kim, D., Cho, Y.H., Ryu, H., Kim, Y., Kim, T.H., and Hwang, I. (2013). BLH1 and KNAT3 modulate ABA responses during germination and early seedling development in Arabidopsis. Plant J. 75: 755-766.
Kimura, S., Koenig, D., Kang, J., Yoong, F.Y., and Sinha, N. (2008). Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr. Biol. 18: 672-677.
Laosatit, K., Amkul, K., Yimram, T., Chen, J., Lin, Y., Yuan, X., Wang, L., Chen, X., and Somta, P. (2022). A Class II KNOX gene, KNAT7-1, regulates physical seed dormancy in mungbean [Vigna radiata (L.) Wilczek]. Front. Plant Sci. 13: 852373.
Li, E., Bhargava, A., Qiang, W., Friedmann, M.C., Forneris, N., Savidge, R.A., Johnson, L.A., Mansfield, S.D., Ellis, B.E., and Douglas, C.J. (2012). The Class II KNOX gene KNAT7 negatively regulates secondary wall formation in Arabidopsis and is functionally conserved in Populus. New Phytol. 194: 102-115.
Li, E., Wang, S., Liu, Y., Chen, J.G., and Douglas, C.J. (2011). OVATE FAMILY PROTEIN4 (OFP4) interaction with KNAT7 regulates secondary cell wall formation in Arabidopsis thaliana. Plant J. 67: 328-341.
Liu, Y., You, S., Taylor-Teeples, M., Li, W.L., Schuetz, M., Brady, S.M., and Douglas, C.J. (2014). BEL1-LIKE HOMEODOMAIN6 and KNOTTED ARABIDOPSIS THALIANA7 interact and regulate secondary cell wall formation via repression of REVOLUTA. Plant Cell 26: 4843-4861.
Magnani, E., and Hake, S. (2008). KNOX lost the OX: The Arabidopsis KNATM gene defines a novel class of KNOX transcriptional regulators missing the homeodomain. Plant Cell 20: 875-887.
Parnis, A., Cohen, O., Gutfinger, T., Hareven, D., Zamir, D., and Lifschitz, E. (1997). The dominant developmental mutants of tomato, Mouse-ear and Curl, are associated with distinct modes of abnormal transcriptional regulation of a Knotted gene. Plant Cell 9: 2143-2158.
Peng, J., Yu, J., Wang, H., Guo, Y., Li, G., Bai, G., and Chen, R. (2011). Regulation of compound leaf development in Medicago truncatula by fused compound leaf1, a class M KNOX gene. Plant Cell 23: 3929-3943.
Rast-Somssich, M.I., Broholm, S., Jenkins, H., Canales, C., Vlad, D., Kwantes, M., Bilsborough, G., Dello Ioio, R., Ewing, R.M., Laufs, P., et al. (2015). Alternate wiring of a KNOXI genetic network underlies differences in leaf development of A. thaliana and C. hirsuta. Gene Dev. 29: 2391-2404.
Reyes-Rivera, J., Rodriguez-Alonso, G., Petrone, E., Vasco, A., Vergara-Silva, F., Shishkova, S., and Terrazas, T. (2017). Expression of the KNOTTED HOMEOBOX genes in the Cactaceae cambial zone suggests their involvement in wood development. Front. Plant Sci. 8: 218.
Sakakibara, K., Ando, S., Yip, H.K., Tamada, Y., Hiwatashi, Y., Murata, T., Deguchi, H., Hasebe, M., and Bowman, J.L. (2013). KNOX2 genes regulate the haploid-to-diploid morphological transition in land plants. Science 339: 1067-1070.
Sakakibara, K., Nishiyama, T., Deguchi, H., and Hasebe, M. (2008). Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development. Evol. Dev. 10: 555-566.
Sakamoto, T., Sakakibara, H., Kojima, M., Yamamoto, Y., Nagasaki, H., Inukai, Y., Sato, Y., and Matsuoka, M. (2006). Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiol. 142: 54-62.
Serikawa, K.A., Martinez-Laborda, A., Kim, H.S., and Zambryski, P.C. (1997). Localization of expression of KNAT3, a class 2 knotted1-like gene. Plant J. 11: 853-861.
Shani, E., Ben-Gera, H., Shleizer-Burko, S., Burko, Y., Weiss, D., and Ori, N. (2010). Cytokinin regulates compound leaf development in tomato. Plant Cell 22: 3206-3217.
Shani, E., Burko, Y., Ben-Yaakov, L., Berger, Y., Amsellem, Z., Goldshmidt, A., Sharon, E., and Ori, N. (2009). Stage-specific regulation of Solanum lycopersicum leaf maturation by class 1 KNOTTED1-LIKE HOMEOBOX proteins. Plant Cell 21: 3078-3092.
Sheng, M., Ma, X., Wang, J., Xue, T., Li, Z., Cao, Y., Yu, X., Zhang, X., Wang, Y., Xu, W., et al. (2022). KNOX II transcription factor HOS59 functions in regulating rice grain size. Plant J. 110: 863-880.
Shwartz, I., Levy, M., Ori, N., and Bar, M. (2016). Hormones in tomato leaf development. Dev. Biol. 419: 132-142.
Sluis, A., and Hake, S. (2015). Organogenesis in plants: Initiation and elaboration of leaves. Trends Genet. 31: 300-306.
Sun, R., Peng, Z., Li, S., Mei, H., Xu, Y., Yang, W., Lu, Z., Wang, H., Zhang, J., and Zhou, C. (2022). Developmental analysis of compound leaf development in Arachis hypogaea. Front. Plant Sci. 13: 749809.
Tadege, M., Wen, J., He, J., Tu, H., Kwak, Y., Eschstruth, A., Cayrel, A., Endre, G., Zhao, P.X., Chabaud, M., et al. (2008). Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J. 54: 335-347.
Truernit, E., Siemering, K.R., Hodge, S., Grbic, V., and Haseloff, J. (2006). A map of KNAT gene expression in the Arabidopsis root. Plant Mol. Biol. 60: 1-20.
Tsuda, K., and Hake, S. (2015). Diverse functions of KNOX transcription factors in the diploid body plan of plants. Curr. Opin. Plant Biol. 27: 91-96.
Wang, H., Chen, J., Wen, J., Tadege, M., Li, G., Liu, Y., Mysore, K.S., Ratet, P., and Chen, R. (2008). Control of compound leaf development by FLORICAULA/LEAFY ortholog SINGLE LEAFLET1 in Medicago truncatula. Plant Physiol. 146: 1759-1772.
Wang, H., Lu, Z., Xu, Y., Zhang, J., Han, L., Chai, M., Wang, Z.Y., Yang, X., Lu, S., Tong, J., et al. (2023). Roles of very long-chain fatty acids in compound leaf patterning in Medicago truncatula. Plant Physiol. 191: 1751-1770.
Wang, L., Lu, W., Ran, L., Dou, L., Yao, S., Hu, J., Fan, D., Li, C., and Luo, K. (2019a). R2R3-MYB transcription factor MYB6 promotes anthocyanin and proanthocyanidin biosynthesis but inhibits secondary cell wall formation in Populus tomentosa. Plant J. 99: 733-751.
Wang, S., Yamaguchi, M., Grienenberger, E., Martone, P.T., Samuels, A.L., and Mansfield, S.D. (2020). The Class II KNOX genes KNAT3 and KNAT7 work cooperatively to influence deposition of secondary cell walls that provide mechanical support to Arabidopsis stems. Plant J. 101: 293-309.
Wang, S., Yang, H., Mei, J., Liu, X., Wen, Z., Zhang, L., Xu, Z., Zhang, B., and Zhou, Y. (2019b). Rice homeobox protein KNAT7 integrates the pathways regulating cell expansion and wall stiffness. Plant Physiol. 181: 669-682.
Wang, X., Zhang, J., Xie, Y., Liu, X., Wen, L., Wang, H., Zhang, J., Li, J., Han, L., Yu, X., et al. (2021). LATE MERISTEM IDENTITY1 regulates leaf margin development via the auxin transporter gene SMOOTH LEAF MARGIN1. Plant Physiol. 187: 218-235.
Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat. Protoc. 2: 1565-1572.
Zhang, Y., Yin, Q., Qin, W., Gao, H., Du, J., Chen, J., Li, H., Zhou, G., Wu, H., and Wu, A.M. (2022). The Class II KNOX family members KNAT3 and KNAT7 redundantly participate in Arabidopsis seed coat mucilage biosynthesis. J. Exp. Bot. 73: 3477-3495.
Zhong, R., Richardson, E.A., and Ye, Z.H. (2007). The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19: 2776-2792.
Zhou, C., Han, L., Hou, C., Metelli, A., Qi, L., Tadege, M., Mysore, K.S., and Wang, Z.Y. (2011). Developmental analysis of a Medicago truncatula smooth leaf margin1 mutant reveals context-dependent effects on compound leaf development. Plant Cell 23: 2106-2124.
Zhou, C., Han, L., Li, G., Chai, M., Fu, C., Cheng, X., Wen, J., Tang, Y., and Wang, Z.Y. (2014). STM/BP-like KNOXI is uncoupled from ARP in the regulation of compound leaf development in Medicago truncatula. Plant Cell 26: 1464-1479.

Auteurs

Xiao Wang (X)

The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Science, Shandong University, Qingdao, 266237, China.

Juanjuan Zhang (J)

The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Science, Shandong University, Qingdao, 266237, China.

Maofeng Chai (M)

Grassland Agri-Husbandry Research Center, College of Grassland Science, Qingdao Agricultural University, Qingdao, 266109, China.

Lu Han (L)

The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Science, Shandong University, Qingdao, 266237, China.

Xiaohua Cao (X)

The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Science, Shandong University, Qingdao, 266237, China.

Jing Zhang (J)

The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Science, Shandong University, Qingdao, 266237, China.

Yiming Kong (Y)

College of Life Sciences, Shandong Normal University, Jinan, 250014, China.

Chunxiang Fu (C)

Key Laboratory of Biofuels, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, 266101, China.

Zeng-Yu Wang (ZY)

Grassland Agri-Husbandry Research Center, College of Grassland Science, Qingdao Agricultural University, Qingdao, 266109, China.

Kirankumar S Mysore (KS)

Institute of Agricultural Biosciences, Oklahoma State University, Ardmore, 73401, Oklahoma, USA.

Jiangqi Wen (J)

Institute of Agricultural Biosciences, Oklahoma State University, Ardmore, 73401, Oklahoma, USA.

Chuanen Zhou (C)

The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Science, Shandong University, Qingdao, 266237, China.

Articles similaires

Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family
Genome, Viral Ralstonia Composting Solanum lycopersicum Bacteriophages
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria

Classifications MeSH