biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 64:385-394, 2020 | DOI: 10.32615/bp.2020.026

Identification and expression pattern analysis of YUCCA and ARF gene families during somatic embryogenesis of Lilium spp.

M.-M. CHEN1, X. LI1, Y.-M. CAI1, Y.-C. ZHANG1, J.-J. GU2, L.-Y. YANG1,*
Faculty of Forestry and Fruit Tree Research Institute, Shanghai Academy of Agricultural Sciences,
1 Shanghai Fengxian District, 201403, P.R. China
2 Shanghai Flower Port Enterprise Development Co., Shanghai 201303, P.R. China

Auxin is a key phytohormone in plant somatic embryogenesis (SE) and YUCCA and AUXIN RESPONSE FACTORS (ARFs) are two key genes involved in auxin biosynthesis and auxin signaling pathways, respectively. They have been reported in participating to the catalytic production of endogenous indole-3-acetic acid (IAA; a natural auxin) and regulating the transcription of auxin-responsive genes. To explore the structural characteristics of the YUCCA and ARF families of Lilium spp. L. and its expression pattern during SE induction and development processes, 6 YUCCA genes and 12 ARF genes were screened from the transcriptome database, and their nucleotides and encoded proteins were analyzed. At the same time, the expression patterns of YUCCA and ARF genes were analyzed by reverse transcription quantitative PCR, and endogenous IAA content was measured. Results show that the members of Lilium indole-3-pyruvate monooxygenase YUCCA (LiYUCs) are structurally conserved among Lilium spp., Oryza sativa, and Arabidopsis thaliana. The LiARFs are classified into six groups, most LiARFs have a closer affinity to the monocotyledon Oryza sativa. All the 12 LiARFs are involved in the SE induction and development, but their expression patterns differed. The LiYUC2/4 and LiARF5/7/21 had expression profiles corresponding with IAA content during the SE induction periods. The LiYUC4/10 and LiARF7/17/18/20/21/22 showed a similar downward trend with IAA content during the progress of the SE development. The results provide a basis for further research on the functions of YUCCA and ARF genes during somatic embryogenesis of Lilium spp.

Keywords: indole-3-acetic acid biosynthesis and signaling pathways, in vitro culture, phylogenetic analysis.

Received: November 15, 2019; Revised: February 11, 2020; Accepted: February 18, 2020; Published online: May 19, 2020  Show citation

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CHEN, M.-M., LI, X., CAI, Y.-M., ZHANG, Y.-C., GU, J.-J., & YANG, L.-Y. (2020). Identification and expression pattern analysis of YUCCA and ARF gene families during somatic embryogenesis of Lilium spp. Biologia plantarum, 64, Article 385-394. https://doi.org/10.32615/bp.2020.026
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    References

    1. Abu-Zaitoon, Y.M., Bennett, K., Normanly, J., Nonhebel, H.M.: A large increase in IAA during development of rice grains correlates with the expression of tryptophan aminotransferase OsTAR1 and a grain-specific YUCCA. - Physiol. Plant. 146: 487-499, 2012. Go to original source...
    2. Ayil-Gutiérrez, B., Galaz-Ávalos, R.M., Peña-Cabrera, E., Loyola-Vargas, V.M.: Dynamics of the concentration of IAA and some of its conjugates during the induction of somatic embryogenesis in Coffea canephora. - Plant Signal Behav. 8: e26998, 2013. Go to original source...
    3. Bai, B., Su, Y.H., Yuan, J., Zhang, X.S.: Induction of somatic embryos in Arabidopsis requires local YUCCA expression mediated by the down-regulation of ethylene biosynthesis. - Mol. Plant 6: 1247-1260, 2013. Go to original source...
    4. Bailey, T.L., Johnson, J., Grant, C.E., Noble, W.S.: The MEME suite. - Nucl. Acids Res. 43: W39-W49, 2015. Go to original source...
    5. Bakhshaie, M., Khosravi, S., Azadi, P., Bagheri, H., Van Tuyl, J.M.: Biotechnological advances in Lilium. - Plant Cell Rep. 35: 1799-1826, 2016. Go to original source...
    6. Bernardi, J., Lanubile, A., Li, Q.B., Kumar, D., Kladnik, A., Cook, S.D., Ross, J.J., Marocco, A., Chourey, P.S.: Impaired auxin biosynthesis in the defective endosperm18 mutant is due to mutational loss of expression in the ZmYuc1 gene encoding endosperm-specific YUCCA1 protein in maize. - Plant Physiol. 160: 1318-1328, 2012. Go to original source...
    7. Carey, N.S., Krogan, N.T.: The role of AUXIN RESPONSE FACTORs in the development and differential growth of inflorescence stems. - Plant Signal Behav. 12: e1307492, 2017. Go to original source...
    8. Chen, M., Zhang, J., Zhou, Y., Li, S., Fan, X., Yang, L., Guan, Y., Zhang, Y.: Transcriptome analysis of Lilium Oriental × Trumpet hybrid roots reveals auxin-related genes and stress-related genes involved in picloram-induced somatic embryogenesis induction. - J. hort. Sci. Biotechnol. 94: 317-330, 2019. Go to original source...
    9. Chen, Q., Dai, X., De Paoli, H., Cheng, Y., Takebayashi, Y., Kasahara, H., Kamiya, Y., Zhao, Y.: Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. - Plant Cell Physiol. 55: 1072-1079, 2014. Go to original source...
    10. Fan, M., Xu, C., Xu, K., Hu, Y.: LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. - Cell Res. 22: 1169-1180, 2012. Go to original source...
    11. Fernando, S.C., Gamage, C.K.A.: Abscisic acid induced somatic embryogenesis in immature embryo explants of coconut (Cocos nucifera L.). - Plant Sci. 151: 193-198, 2000. Go to original source...
    12. Gallavotti, A., Barazesh, S., Malcomber, S., Hall, D., Jackson, D., Schmidt, R.J., McSteen, P.: sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize. - Proc. nat. Acad. Sci. USA. 105: 15196-15201, 2008. Go to original source...
    13. Guilfoyle, T.J., Hagen, G.: Auxin response factors. - Curr. Opin. Plant Biol. 10: 453-460, 2007. Go to original source...
    14. Hagen, G., Guilfoyle, T.: Auxin-responsive gene expression: genes, promoters and regulatory factors. - Plant mol. Biol. 49: 373-385, 2002. Go to original source...
    15. Ikeuchi, M., Favero, D.S., Sakamoto, Y., Iwase, A., Coleman, D., Rymen, B., Sugimoto, K.: Molecular mechanisms of plant regeneration. - Annu. Rev. Plant Biol. 70: 3.1-3.30, 2019. Go to original source...
    16. Jain, S.M., Gupta, P.K., Newton, R.J. Somatic Embryogenesis in Woody Plants. - Springer Science & Business Media, Berlin 2013.
    17. Kefford, N.P., Caso, O.H.: A potent auxin with unique chemical structure - 4-amino-3,5,6-trichloropicolinic acid. -Bot. Gaz. 127: 159-163, 1966. Go to original source...
    18. Kim, J.I., Baek, D., Park, H.C., Chun, H.J., Oh, D.H., Lee, M.K., Cha, J.Y., Kim, W.Y., Kim, M.C., Chung, W.S., Bohnert, H.J., Lee, S.Y., Bressan, R.A., Lee, S.W., Yun, D.J.: Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit. - Mol. Plant 6: 337-349, 2013. Go to original source...
    19. Kumar, R., Tyagi, A.K., Sharma, A.K.: Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. - Mol. Genet. Genomics 285: 245-260, 2011. Go to original source...
    20. Lee, K., Seo, P.J.: High-temperature promotion of callus formation requires the BIN2-ARF-LBD axis in Arabidopsis. -Planta 246: 797-802, 2017. Go to original source...
    21. Lin, Y., Lai, Z., Tian, Q., Lin, L., Lai, R., Yang, M., Zhang, D., Chen, Y., Zhang, Z.: Endogenous target mimics down-regulate miR160 mediation of ARF10, -16, and -17 cleavage during somatic embryogenesis in Dimocarpus longan Lour. - Front Plant Sci. 6: 956, 2015. Go to original source...
    22. Liu, H., Xie, W.F., Zhang, L., Valpuesta, V., Ye, Z.W., Gao, Q.H., Duan, K.: Auxin biosynthesis by the YUCCA6 flavin monooxygenase gene in woodland strawberry (Fragaria vesca). - J. integr. Plant Biol. 56: 350-363, 2014. Go to original source...
    23. Liu, S., Chen, W., Qu, L., Gai, Y., Jiang, X.: Simultaneous determination of 24 or more acidic and alkaline phytohormones in femtomole quantities of plant tissues by high-performance liquid chromatography-electrospray ionization-ion trap mass spectrometry. - Anal. bioanal. Chem. 405: 1257-1266, 2013. Go to original source...
    24. Liu, Z., Miao, L., Huo, R., Song, X., Johnson, C., Kong, L., Sundaresan, V., Yu, X.: ARF2-ARF4 and ARF5 are essential for female and male gametophyte development in Arabidopsis. - Plant Cell Physiol. 59: 179-189, 2018. Go to original source...
    25. Mano, Y., Nemoto, K.: The pathway of auxin biosynthesis in plants. - J. exp. Bot. 63: 2853-2872, 2012. Go to original source...
    26. Mashiguchi, K., Tanaka, K., Sakai, T., Sugawara, S., Kawaide, H., Natsume, M., Hanada, A., Yaeno, T., Shirasu, K., Yao, H., McSteen, P., Zhao, Y., Hayashi, K., Kamiya, Y., Kasahara, H.: The main auxin biosynthesis pathway in Arabidopsis. - Proc. nat. Acad. Sci. USA 108: 18512-18517, 2011. Go to original source...
    27. Michalczuk, L., Ribnicky, D.M., Cooke, T.J., Cohen, J.D.: Regulation of indole-3-acetic acid biosynthetic pathways in carrot cell cultures. - Plant Physiol. 100:1346-1353, 1992. Go to original source...
    28. Pan, X., Welti, R., Wang, X.: Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. - Nature Protoc. 5: 986-992, 2010. Go to original source...
    29. Peng, J., Berbel, A., Madueño, F., Chen, R.: AUXIN RESPONSE FACTOR3 regulates compound leaf patterning by directly repressing PALMATE-LIKE PENTAFOLIATA1 expression in Medicago truncatula. - Front Plant Sci. 8: 1630, 2017. Go to original source...
    30. Pescador, R., Kerbauy, G.B., Melo Ferreira, W., Purgatto, E., Suzuki, R.M., Guerra, M.P.: A hormonal misunderstanding in Acca sellowiana embryogenesis: levels of zygotic embryogenesis do not match those of somatic embryogenesis. - Plant Growth Regul. 68: 67-76, 2012. Go to original source...
    31. Poulet, A., Kriechbaumer, V.: Bioinformatics analysis of phylogeny and transcription of TAA/YUC auxin biosynthetic genes. - Int. J. mol. Sci. 18: 1791, 2017. Go to original source...
    32. Prado, M.J., Largo, A., Domínguez, C., Gonzálezc, M.V., Reya, M. Centeno, M.L.: Determination of abscisic acid and its glucosyl ester in embryogenic callus cultures of Vitis vinifera in relation to the maturation of somatic embryos using a new liquid chromatography ELISA analysis method. - J. Plant Physiol. 171: 852-859, 2014. Go to original source...
    33. Remington, D.L., Vision, T.J., Guilfoyle, T.J., Reed, J.W.: Contrasting modes of diversification in the Aux/IAA and ARF gene families. - Plant Physiol. 135: 1738-1752, 2004. Go to original source...
    34. Ren, Z., Liu, R., Gu, W., Dong, X.: The Solanum lycopersicum auxin response factor SlARF2 participates in regulating lateral root formation and flower organ senescence. - Plant Sci. 256: 103-111, 2017. Go to original source...
    35. Roodbarkelari, F., Du, F., Truernit, E., Laux, T.: ZLL/AGO10 maintains shoot meristem stem cells during Arabidopsis embryogenesis by down-regulating ARF2-mediated auxin response. - BMC Biol. 13: 74, 2015. Go to original source...
    36. Shen, C., Yue, R., Sun, T., Zhang, L., Xu, L., Tie, S., Wang, H., Yang, Y.: Genome-wide identification and expression analysis of auxin response factor gene family in Medicago truncatula. - Front Plant Sci. 6: 73, 2015. Go to original source...
    37. Song, S., Wang Z., Ren Y., Sun H.: Full-length transcriptome analysis of the ABCB, PIN/PIN-LIKES, and AUX/LAX families involved in somatic embryogenesis of Lilium pumilum DC. Fisch. - Int. J. mol. Sci. 21: 453, 2020. Go to original source...
    38. Stone, S.L., Braybrook, S.A., Paula, S.L., Kwong, L.W., Meuser, J., Pelletier, J., Hsieh, T.F., Fischer, R.L., Goldberg, R.B., Harada, J.J.: Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. - PNAS 105: 3151-3156, 2008. Go to original source...
    39. Su, Y.H., Zhao, X.Y., Liu, Y.B., Zhang, C.L., O'Neill, S.D., Zhang, X.S.: Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. - Plant J. 59: 448-460, 2009. Go to original source...
    40. Sun, R.B., Wang, S.H., Ma, D., Li, Y.L., Liu, C.L.: Genome-wide analysis of cotton auxin early response gene families and their roles in somatic embryogenesis. - Genes 10: 730, 2019. Go to original source...
    41. Tian, L., Brown, D.C.W.: Improvement of soybean somatic embryo development and maturation by abscisic acid treatment. - Can. J. Plant Sci. 80: 271-276, 2000. Go to original source...
    42. Tiwari, S.B., Wang, X.J., Hagen, G., Guilfoyle, T.J.: Aux/IAA proteins are active repressors and their stability and activity are modulated by auxin. - Plant Cell 13: 2809-2822, 2001. Go to original source...
    43. Tobeña-Santamaria, R., Bliek, M., Ljung, K., Sandberg, G., Mol, J.N., Souer, E., Koes, R.: FLOOZY of petunia is a flavin mono-oxygenase-like protein required for the specification of leaf and flower architecture. - Genes Dev. 16: 753-763, 2002. Go to original source...
    44. Ulmasov, T., Hagen, G., Guilfoyle, T.J.: Dimerization and DNA binding of auxin response factors. - Plant J. 19: 309-319, 1999. Go to original source...
    45. Vondráková, Z., Eliá¹ová, K., Fischerová, L., Vágner, M.: The role of auxins in somatic embryogenesis of Abies alba. - Cent. Eur. J. Biol. 6: 587-596, 2011. Go to original source...
    46. Wang, D., Pei, K., Fu, Y., Sun, Z., Li, S., Liu, H., Tang, K., Han, B., Tao, Y.: Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). - Gene 394: 13-24, 2007. Go to original source...
    47. Wang, W., Gu, L., Ye, S., Zhang, H., Cai, C., Xiang, M., Gao, Y., Wang, Q., Lin, C., Zhu, Q.: Genome-wide analysis and transcriptomic profiling of the auxin biosynthesis, transport and signaling family genes in moso bamboo (Phyllostachys heterocycla). - BMC Genomics 18: 870, 2017. Go to original source...
    48. Wójcikowska, B., Gaj, M.D.: Expression profiling of AUXIN RESPONSE FACTOR genes during somatic embryogenesis induction in Arabidopsis. -Plant Cell Rep. 36: 843-858, 2017. Go to original source...
    49. Wójcikowska, B., Jaskó³a, K., Gasiorek, P., Meus, M., Nowak, K., Gaj, M.D.: LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis. - Planta 238: 425-440, 2013. Go to original source...
    50. Won, C., Shen, X., Mashiguchi, K., Zheng, Z., Dai, X., Cheng, Y., Kasahara, H., Kamiya, Y., Chory, J., Zhao, Y.: Conversion of tryptophan to indole-3-acetic acid by tryptophan aminotransferases of Arabidopsis and YUCCAs in Arabidopsis. - Proc. nat. Acad. Sci. USA 108: 18518-18523, 2011. Go to original source...
    51. Yamamoto, Y., Kamiya, N., Morinaka, Y., Matsuoka, M., Sazuka, T.: Auxin biosynthesis by the YUCCA genes in rice. - Plant Physiol. 143: 1362-1371, 2007. Go to original source...
    52. Yi, J., Liu, L., Cao, Y., Li, J., Mei, M.: Cloning, characterization and expression of OsFMO(t) in rice encoding a flavin monooxygenase. - J. Genet. 92: 471-480, 2013. Go to original source...
    53. Zavattieri, M.A., Frederico, A.M., Lima, M., Sabino, R., Arnholdt-Schmitt, B.: Induction of somatic embryogenesis as an example of stress-related plant reactions. - Electr. J. Biotechnol. 13: 12-13, 2010. Go to original source...
    54. Zhang, J., Gai, M.Z., Li, X.L., Li, T.L., Sun, H.M.: Somatic embryogenesis and direct as well as indirect organogenesis in Lilium pumilum DC. Fisch., an endangered ornamental and medicinal plant. - Biosci. Biotechnol. Biochem. 80: 1898-1906, 2016. Go to original source...
    55. Zhang, L.F., Li, W.F., Xu, H.Y., Qi, L.W., Han, S.Y.: Cloning and characterization of four differentially expressed cDNAs encoding NFYA homologs involved in responses to ABA during somatic embryogenesis in Japanese larch (Larix leptolepis). - Plant Cell Tissue Organ Cult. 117: 293-304, 2014. Go to original source...
    56. Zhou, X.H., Zheng, R.H., Liu, G.X., Xu, Y., Zhou, Y.W., Laux, T., Zhen, Y., Harding, S.A., Shi, J.S., Chen, J.H.: Desiccation treatment and endogenous IAA levels are key factors influencing high frequency somatic embryogenesis in Cunninghamia lanceolata (Lamb.) Hook. - Front Plant Sci. 8: 2054, 2017. Go to original source...
    57. Zhou, Y., Zhang, J., Chen, M., Gu, J. Development of plant regeneration system via somatic embryogenesis from roots of Lilium hybrid cultivars. - Propag. ornamental Plants 13: 130-137, 2013.

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