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Further insight into the role of KAN1, a member of KANADI transcription factor family in rice

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Abstract

The rice EMS-derived mutant leaf adaxialized 1 (lad1) was isolated based on its upward rolling leaf phenotype. Besides the adaxially rolled leaf, many other agronomic traits were also compromised in lad1. The rolling trait was characterized by a noticeable alteration of bulliform cells in the adaxial side of the leaves. Map-based cloning showed a single nucleotide substitution in the promoter region of the KAN1 gene in lad1 mutant. Further, over-expressing and CRISPR/cas9-edited knockdown transgenic plants confirmed that KAN1 was responsible for the mutant phenotype of lad1. Yeast two-hybrid and bimolecular fluorescence complementation assay demonstrated that KAN1 can interact with the auxin response factors ARF3, ARF7 and ARF15. Physiologically, the contents of auxin (IAA), abscisic acid (ABA), jasmonic acid (JA) and gibberellin (GA) were all significantly increased in the lad1 mutant. Moreover, the GA3 content dramatically decrease in wild-type, but increased in lad1 under IAA induction. Additionally, the expression levels of several IAA and GA biosynthesis and responsive-related genes and genes involved in leaf polarity determination were altered in lad1. Therefore, we hypothesized that KAN1/ARFs protein complexes act as auxin-dependent regulatory units that play a conserved role in leaf development.

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References

  • Bentsink L, Koornneef M (2008) Seed dormancy and germination. The arabidopsis book, Somerville CR, Meyerowitz EM (eds) American Society of Plant Biologists, Rockville

    Google Scholar 

  • Bunger-Kibler, Bangerth F (1982) Relationship between cell number, cell size and fruit size of seeded fruits of tomato (Lycopersicon esculentum Mill.), and those induced parthenocarpically by the application of plant growth regulators. Plant Growth Regul 1:143–154

    Google Scholar 

  • Candela H, Johnston R, Gerhold A, Foster T, Hake S (2008) The milkweed pod1 gene encodes a KANADI protein that is required for abaxial/adaxial patterning in maize leaves. Plant Cell 8:2073–2087

    Article  Google Scholar 

  • Cerkauskas R (2004) Pepper disease verticillium wilt, AVRDC Publication, Shanhua, pp 04–581

    Google Scholar 

  • Chen QL, Xie QJ, Gao J, Wang WY, Sun B, Liu BH, Zhu HT, Peng HF, Zhao HB, Liu CH, Wang J, Zhang JL, Zhang GQ, Zhang ZM (2015) Characterization of rolled and erect leaf 1 in regulating leave morphology in rice. J Exp Bot 66:6047–6058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009) The Solanumlycopersicum.LAUXIN RESPONSE FACTOR 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57:160–170

    Article  PubMed  Google Scholar 

  • De Jong M, Wolters-Arts M, García-Martínez JL, Mariani C, Vriezen WH (2011) The Solanumlycopersicum.L AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signalling during tomato fruit set and development. J Exp Bot 62:617–626

    Article  PubMed  Google Scholar 

  • Dorcey E, Urbez C, Blazquez MA, Carbonell J, Perez-Amador MA (2009) Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. The Plant J 58:318–332

    Article  CAS  PubMed  Google Scholar 

  • Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260

    Article  CAS  PubMed  Google Scholar 

  • Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131:2997–3006

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415

    Article  CAS  PubMed  Google Scholar 

  • Frigerio M, Alabad D, Perez-Gomez J, Garcıa-Carcel L, Phillips AL, Hedden P, Blazquez MA (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in arabidopsis. Plant Physiol 142:553–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao YW (2014) Auxin-mediated fruit development and ripening: New insight on the role of Arfs and their action mechanism in Tomato (S. lycopersicum). Doctoral Thesis: Institut National Polytechnique de Toulouse (INP Toulouse) pp 174

  • Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E (1996) The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84:735–744

    Article  CAS  PubMed  Google Scholar 

  • Hawker NP. Bowman JL (2004) Roles for class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Phys 135:2261–2270

    Article  CAS  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  CAS  PubMed  Google Scholar 

  • Izhaki A, Bowman JL (2007) KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell 19:495–508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson D, Veit B, Hake S (1994) Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120:405–413

    CAS  Google Scholar 

  • Kadioglu A, Terzi R (2007) A dehydration avoidance mechanism: leaf rolling. Bot Rev 73:290–302

    Article  Google Scholar 

  • Kant S, Bi YM, Zhu T, Rothstein SJ (2009) SAUR39, a small auxin-Up RNA Gene, acts as a negative regulator of auxin synthesis and transport in rice. Plant Physiol 151:691–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley DR, Arreola A, Gallagher TL, Gasser CS (2012) ETTIN (ARF3) physically interacts with KANADI proteins to form a functional complex essential for integument development and polarity determination in Arabidopsis. Development 139:1105–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Xu L, Wang H, Yuan Z, Cao X, Yang Z, Zhang D, Xu Y, Huang H (2005) The putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and microRNA165/166 in Arabidopsis leaf development. Plant Cell 17:2157–2171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S (1994) A knotted1-likehomeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6:1859–1876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XD, Zhang H, Zhao Y, Feng ZY, Li Q, Yang HQ, Luan S, Li JM, He ZH (2013) Auxin controls seed dormancy through stimulationof abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci USA 110:15485–15490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma XL, Zhang QY, Zhu QL, Liu W, Chen Y, Qiu R, Wang B, Yang ZF, Li HY, Lin YR, Xie YY, Shen RX, Chen SF, Wang Z, Chen YL, Guo JX, Chen LT, Zhao XC, Dong ZC, Liu YG (2015) A Robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8:1274–1284

    Article  CAS  PubMed  Google Scholar 

  • Merelo P, Xie YK, Brand L, Ott F, Weigel D, Bowman JL, Heisler MG, Wenkel S (2013) Genome-wide identification of KANADI1 target genes. PLoS ONE 8(10):e77341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118

    Article  CAS  PubMed  Google Scholar 

  • Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, Okada K (2012) Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell 24:519–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Toole JC, Cruz RT (1980) Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. Plant Physiol 65:428–432

    Article  PubMed  PubMed Central  Google Scholar 

  • Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Sage Public 2:121–136

    Google Scholar 

  • Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribnicky DM, Nebojsa I, Cohen JD, Cooke TJ (1996) The effects of exogenous auxins on endogenous indole-3-acetic acid metabolism: the implications for carrot somatic embryogenesis. Plant Physiol 112:549–558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarieva GE, Kenzhebaeva SS, Lichtenthaler HK (2010) Adaptation potential of photosynthesis in wheat cultivars with a capability of leaf rolling under high temperature conditions. Russ J Plant Physiol 57:28–36

    Article  CAS  Google Scholar 

  • Serrani JC, Sanjuán R, Ruiz-Rivero O, Fos M, Garcίa-Martίnez JL (2007) Gibberellin regulation of fruit set and growth in tomato. Plant Physiol 145:246–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shields LM (1951) The involution mechanism in leaves of certain xeric grasses. Phytomorphology 1(1):225–241

    Google Scholar 

  • Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128

    CAS  PubMed  Google Scholar 

  • Subashri M, Robin S, Vinod KK, Rajeswari S, Mohanasundaram K, Raveendran TS (2009) Trait identification and QTL validation for reproductive stage drought resistance in rice using selective genotyping of near flowering RILs. Euphytica 166:291–305

    Article  Google Scholar 

  • Tanaka W, Toriba T, Ohmori Y, Yoshida A, Kawai A, Mayama-Tsuchida T, Ichikawa H, Mitsuda N, Ohme-Takagl M, Hirano HY (2012) The YABBY gene TONGARI-BOUSHI1 is involved in lateral organ development and maintenance of meristem organization in the rice spikelet. Plant Cell 124:80–95

    Article  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    Article  CAS  PubMed  Google Scholar 

  • Trapp MA, De Souza GD, Rodrigues-Filho E, Boland W, Mithöfer A (2014) Validated method for phytohormone quantification in plants. Front Plant Sci 5:417

    Google Scholar 

  • Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YI, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Hua D, He J, Duan Y, Chen Z, Hong X, Gong Z (2011) Auxin response Factor2 (ARF2) and its regulated homeodomain gene HB33 mediate abscisic acid response in Arabidopsis. PLoS Genet 7:e1002172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei XJ, Tang SQ, Shao GN, Chen ML, Hu YC, Hu PS (2013) Fine mapping and characterization of a novel dwarf and narrow-leaf mutant dnl1 in rice. Genet Mol Res 12:3845–3855

    Article  CAS  PubMed  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi T, Nukazuka A, Tsukaya H (2012) Leaf adaxial–abaxial polarity specification and lamina outgrowth: evolution and development. Plant Cell Physiol 53:1180–1194

    Article  CAS  PubMed  Google Scholar 

  • Yan CJ, Yan S, Zhang ZQ, Liang GH, Lu JF, Gu MH (2006) Genetic analysis and gene fine mapping for a rice novel mutant rl9(t) with rolling leaf character. Chin Sci Bull 51:63–69

    Article  Google Scholar 

  • Yang CM (2010) Assessment of the severity of bacterial leaf blight in rice using canopy hyperspectral reflectance. Prec Agric 11:61–81

    Article  Google Scholar 

  • Yoshikawa T, Eiguchi M, Hibara KI, Ito JI, Nagato Y (2013) Rice SLENDER LEAF1 gene encodes cellulose synthase-likeD4 and is specifically expressed in M-phase cells to regulate cell proliferation. J Exp Bot 64:2049–2061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang GH, Xu Q, Zhu XD, Qian Q, Xue HW (2009) SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21:719–735

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao SQ, Xiang JJ, Xue HW (2013) Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amidoSynthetase, reveal the effects of auxin in leaf inclination control. Mol Plant 6:174–187

    Article  CAS  PubMed  Google Scholar 

  • Zhao JF, Wang T, Wang MX, Liu YY, Yuan SJ, Gao YN, Yin L, Sun W, Peng LX, Zhang WH, Wan JM, Li XY (2014) DWARF3 participates in an SCF complex and associates with DWARF14 to suppress rice shoot branching. Plant Cell Physiol 6:1096–1109

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (2016YFD0101801), the National Natural Science Foundation of China (31501285, 31521064), and by the National S&T Major Project of China (2016ZX08001006).

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YMNA, BF and LS performed the experiments. YMNA and XW analyzed the data. PH and XW designed the project. YMNA and XW draft the manuscript. ZS and ST performed a critical revision of the article. All authors read and approved the final manuscript.

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Correspondence to Xiangjin Wei or Peisong Hu.

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Adedze, Y.M.N., Feng, B., Shi, L. et al. Further insight into the role of KAN1, a member of KANADI transcription factor family in rice. Plant Growth Regul 84, 237–248 (2018). https://doi.org/10.1007/s10725-017-0335-7

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