Auxin-induced AUXIN RESPONSE FACTOR4 activates APETALA1 and FRUITFULL to promote flowering in woodland strawberry

Xiangxiang Dong , Yanjun Li , Yuhan Guan , Shaoxi Wang , He Luo , Xiaoming Li , He Li , Zhihong Zhang

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 115

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :115 DOI: 10.1038/s41438-021-00550-x
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Auxin-induced AUXIN RESPONSE FACTOR4 activates APETALA1 and FRUITFULL to promote flowering in woodland strawberry
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Abstract

Flowering time is known to be regulated by numerous pathways, such as the autonomous, gibberellin, aging, photoperiod-mediated, and vernalization pathways. These regulatory mechanisms involve both environmental triggers and endogenous hormonal cues. Additional flowering control mechanisms mediated by other phytohormones, such as auxin, are less well understood. We found that in cultivated strawberry (Fragaria × ananassa), the expression of auxin response factor4 (FaARF4) was higher in the flowering stage than in the vegetative stage. Overexpression of FaARF4 in Arabidopsis thaliana and woodland strawberry (Fragaria vesca) resulted in transgenic plants flowering earlier than control plants. In addition, FveARF4-silenced strawberry plants showed delayed flowering compared to control plants, indicating that FaARF4 and FveARF4 function similarly in regulating flowering. Further studies showed that ARF4 can bind to the promoters of the floral meristem identity genes APETALA1 (AP1) and FRUITFULL (FUL), inducing their expression and, consequently, flowering in woodland strawberry. Our studies reveal an auxin-mediated flowering pathway in strawberry involving the induction of ARF4 expression.

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Xiangxiang Dong, Yanjun Li, Yuhan Guan, Shaoxi Wang, He Luo, Xiaoming Li, He Li, Zhihong Zhang. Auxin-induced AUXIN RESPONSE FACTOR4 activates APETALA1 and FRUITFULL to promote flowering in woodland strawberry. Horticulture Research, 2021, 8 (1) : 115 DOI:10.1038/s41438-021-00550-x

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References

[1]

Kinmonth-Schultz, H. A. et al. Cool night-time temperatures induce the expression of CONSTANS and FLOWERING LOCUS T to regulate flowering in Arabidopsis. New Phytol. 211, 208-224 (2016).

[2]

Lin, T. et al. VcRR2 regulates chilling-mediated flowering through expression of hormone genes in a transgenic blueberry mutant. Hortic. Res. 6, 96 (2019).

[3]

Berding, N. & Hurney, A. P. Flowering and lodging, physiological-based traits affecting cane and sugar yield: what do we know of their control mechanisms and how do we manage them? Field Crops Res. 92, 261-275 (2005).

[4]

Shojaei, E., Mirzaie-Asl, A., Mahmoudi, S. B. & Nazeri, S. Identification of sugar beet flowering genes based on Arabidopsis homologous genes. J. Agr. Sci. Tech. 19, 719-729 (2017).

[5]

Ma, Z.B., Li, W., Wang, H.P. & Yu, D.Q. WRKY transcription factors WRKY12 and WRKY13 interact with SPL10 to modulate age-mediated flowering. J. Integr. Plant Biol. 62, 1659-1673 (2020).

[6]

Teotia, S. & Tang, G. To bloom or not to bloom, role of microRNAs in plant flowering. Mol. Plant 8, 359-377 (2015).

[7]

Liu, Y. X. et al. Over-expression of EjLFY1 leads to an early flowering habit in strawberry (Fragaria × ananassa) and its asexual progeny . Front. Plant Sci. 8, 496 (2017).

[8]

Lu, J. et al. Alternate expression of CONSTANS-LIKE 4 in short days and CONSTANS in long days facilitates day-neutral response in Rosa chinensis . J. Exp. Bot. 71, 4057-4068 (2020).

[9]

Lanctot, A. & Nemhauser, J. L. It’s Morphin’ time: how multiple signals converge on ARF transcription factors to direct development. Curr. Opin. Plant Biol. 57, 1-7 (2020).

[10]

Fahlgren, N. et al. Regulation of auxin response factor3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr. Biol. 16, 939-944 (2006).

[11]

Kalve, S. et al. Osmotic stress inhibits leaf growth of Arabidopsis thaliana by enhancing ARF-mediated auxin responses. New Phytol. 226, 1766-1780 (2020).

[12]

Fan, S. H. et al. Molecular functional analysis of auxin/indole-3-acetic acid proteins (Aux/IAAs) in plant disease resistance in cassava. Physiol. Plant. 168, 88-97 (2020).

[13]

John, W. C. Auxin response factors. Plant Cell Environ. 39, 1014-1028 (2016).

[14]

Goetz, M., Vivian-Smith, A., Johnson, S. D. & Koltunow, A. M. AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 18, 1873-1886 (2006).

[15]

Narise, T. et al. Involvement of auxin signaling mediated by IAA14 and ARF7/19 in membrane lipid remodeling during phosphate starvation. Plant Mol. Biol. 72, 533-544 (2010).

[16]

Hardtke, C. S. et al. Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL4. Development 131, 1089-1100 (2004).

[17]

Gasciolli, V., Mallory, A. C., Bartel, D. P. & Vaucheret, H. Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15, 1494-1500 (2005).

[18]

Koskela, E. A. et al. Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca . Plant Physiol. 159, 1043-1054 (2012).

[19]

Li, C. J., Yamagishi, N., Kasajima, I. & Yoshikawa, N. Virus-induced gene silencing and virus-induced flowering in strawberry (Fragaria × ananassa) using apple latent spherical virus vectors . Hortic. Res. 6, 18 (2019).

[20]

Cao, F. et al. Expression and functional analysis of FaPHO1;H9 gene of strawberry (Fragaria × ananassa) . J. Integr. Agr. 15, 60345-60357 (2017).

[21]

Eikemo, H. & Brurberg, M. B. Resistance to Phytophthora cactorum in diploid Fragaria species . Hort. Science 45, 193-197 (2010).

[22]

Slovin, J. P., Schmitt, K. & Folta, K. M. An inbred line of the diploid strawberry Fragaria vesca f. semperflorens for genomic and molecular genetic studies in the Rosaceae . Plant Methods 5, 15 (2009).

[23]

Li, Y. P., Pi, M. T., Gao, Q., Liu, Z. C. & Kang, C. Y. Updated annotation of the wild strawberry Fragaria vesca V4 genome. Hortic. Res. 6, 61 (2019).

[24]

Li, H. et al. Tissue culture responsive MicroRNAs in strawberry. Plant Mol. Biol. Rep. 30, 1047-1054 (2012).

[25]

Li, H., Zhang, Z. H., Huang, F. F., Chang, L. L. & Ma, Y. MicroRNA expression profiles in conventional and micropropagated strawberry (Fragaria × ananassa Duch.) plants . Plant Cell Rep. 28, 891-902 (2009).

[26]

Li, H., Dong, X. X., Mao, W. J., Guan, Y. H. & Zhang, Z. H. An effective artificial microRNA vector based on Fv-miR166 precursor from strawberry. Sci. Hortic. 256, 108643 (2019).

[27]

Fait, A. et al. Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiol. 148, 730-750 (2008).

[28]

Picard, V., Ersdal-Badju, E., Lu, A. & Bock, S. C. A rapid and efficient one-tube PCR-based mutagenesis technique using Pfu DNA polymerase. Nucleic Acids Res. 22, 2587-2591 (1994).

[29]

Ghelli, R. et al. A newly identified flower-specific splice variant of AUXIN RESPONSE FACTOR8 regulates stamen elongation and endothecium lignification in Arabidopsis. Plant Cell 303, 620-637 (2018).

[30]

Meland, M., Frøynes, O., Coop, L. & Kaiser, C. Modeling of sweet cherry flowering based on temperature and phenology in a mesic Nordic climate. Acta Hortic. 1162, 19-22 (2017).

[31]

Cardoso, J. C., Martinelli, A. P. & Silva, J . A novel approach for the selection of Cattleya hybrids for precocious and season-independent flowering . Euphytica 210, 143-150 (2016).

[32]

Tenreira, T. et al. A specific gibberellin 20-oxidase dictates the flowering-runnering decision in diploid strawberry. Plant Cell 29, 2168-2182 (2017).

[33]

Zahedi, S. M. & Sarikhani, H. The effect of end of day far-red light on regulating flowering of short-day strawberry (Fragaria × ananassa Duch. сv. Paros) in a long-day situation . Russ. J. Plant Physiol. 64, 83-90 (2017).

[34]

Hidaka, K., Dan, K., Imamura, H. & Takayama, T. Crown-cooling treatment induces earlier flower bud differentiation of strawberry under high air temperatures. Environ. Control Biol. 55, 21-27 (2017).

[35]

Al-madhagi, I. A. H., Hasan, S. M. Z., bin Ahmad, A., Zain, A. M. & bin Yusoff, W. A. The influence of exogenous hormone on the flowering and fruiting of strawberry (Fragaria × ananassa Duch.) . J. Biol. Agric. Health. 2, 46-53 (2012).

[36]

Li, S. B. et al. Genome-wide identification, isolation and expression analysis of auxin response factor (ARF) gene family in sweet orange (Citrus sinensis) . Front. Plant Sci. 6, 119 (2015).

[37]

Shen, C. J. et al. Genome-wide identification and expression analysis of auxin response factor gene family in Medicago truncatula . Front. Plant Sci. 6, 73 (2015).

[38]

Liu, N. N. et al. Genome-wide identification, molecular evolution, and expression analysis of auxin response factor (ARF) gene family in Brachypodium distachyon L. BMC Plant Biol. 18, 336 (2018).

[39]

Wang, S. X. et al. Genome-wide identification and expression analysis of auxin response factor (ARF) gene family in strawberry (Fragaria vesca) . J. Integr. Agr. 18, 1587-1603 (2019).

[40]

Chen, L. et al. Soybean AP1 homologs control flowering time and plant height. J. Integr. Plant Biol. 62, 1868-1879 (2020).

[41]

Leseberg, C. H. et al. Interaction study of MADS-domain proteins in tomato. J. Exp. Bot. 59, 2253-2265 (2008).

[42]

Danilevskaya, O. N. et al. Involvement of the MADS-box gene ZMM4 in floral induction and inflorescence development in maize. Plant Physiol. 147, 2054-2069 (2008).

[43]

Cevik, V. et al. A FRUITFULL-like gene is associated with genetic variation for fruit flesh firmness in apple (Malus domestica Borkh.) . Tree Genet. Genomes 6, 271-279 (2010).

[44]

Chang, L. L., Zhang, Z. H., Yang, H., Li, H. & Dai, H. Y. Detection of strawberry RNA and DNA viruses by RT-PCR using total nucleic acid as a template. J. Phytopathol. 155, 431-436 (2007).

[45]

Li, W. J. et al. FveRGA1, encoding a DELLA protein, negatively regulates runner production in Fragaria vesca . Planta 247, 941-951 (2018).

[46]

Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729 (2013).

[47]

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method . Methods 25, 402-408 (2001).

[48]

Zhang, F. et al. MdWRKY100 encodes a group I WRKY transcription factor in Malus domestica that positively regulates resistance to Colletotrichum gloeosporioides infection . Plant Sci. 286, 68-77 (2019).

[49]

Chen, K. Q. et al. MdMYB46 could enhance salt and osmotic stress tolerance in apple by directly activating stress-responsive signals . Plant Biotechnol. J. 17, 2341-2355 (2019).

[50]

Li, T. et al. The jasmonate-activated transcription factor MdMYC2 regulates ETHYLENE RESPONSE FACTOR and ethylene biosynthetic genes to promote ethylene biosynthesis during apple fruit ripening. Plant Cell 29, 1316-1334 (2017).

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