The red/far-red light photoreceptor FvePhyB regulates tissue elongation and anthocyanin accumulation in woodland strawberry

Qi Gao , Shaoqiang Hu , Xiaoli Wang , Fu Han , Huifeng Luo , Zhongchi Liu , Chunying Kang

Horticulture Research ›› 2023, Vol. 10 ›› Issue (12) : 232

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (12) :232 DOI: 10.1093/hr/uhad232
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The red/far-red light photoreceptor FvePhyB regulates tissue elongation and anthocyanin accumulation in woodland strawberry
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Abstract

Light is an important environmental signal that influences plant growth and development. Among the photoreceptors, phytochromes can sense red/far-red light to coordinate various biological processes. However, their functions in strawberry are not yet known. In this study, we identified an EMS mutant, named P8, in woodland strawberry (Fragaria vesca) that showed greatly increased plant height and reduced anthocyanin content. Mapping-by-sequencing revealed that the causal mutation in FvePhyB leads to premature termination of translation. The light treatment assay revealed that FvePhyB is a bona fide red/far-red light photoreceptor, as it specifically inhibits hypocotyl length under red light. Transcriptome analysis showed that the FvePhyB mutation affects the expression levels of genes involved in hormone synthesis and signaling and anthocyanin biosynthesis in petioles and fruits. The srl mutant with a longer internode is caused by a mutation in the DELLA gene FveRGA1 (Repressor of GA1) in the gibberellin pathway. We found that the P8 srl double mutant has much longer internodes than srl, suggesting a synergistic role of FvePhyB and FveRGA1 in this process. Taken together, these results demonstrate the important role of FvePhyB in regulating plant architecture and anthocyanin content in woodland strawberry.

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Qi Gao, Shaoqiang Hu, Xiaoli Wang, Fu Han, Huifeng Luo, Zhongchi Liu, Chunying Kang. The red/far-red light photoreceptor FvePhyB regulates tissue elongation and anthocyanin accumulation in woodland strawberry. Horticulture Research, 2023, 10 (12) : 232 DOI:10.1093/hr/uhad232

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Acknowledgements

We thank Dr Hongli Lian (Shanghai Jiao Tong University) for comments on the manuscript. This work was supported by the National Natural Science Foundation of China (32172539) and the Fundamental Research Funds for the Central Universities (2662022YLPY002).

Author contributions

Q.G. and C.K. conceived and designed the experiments. Q.G., S.H., X.W., F.H., and H.L. performed the experiments. Z.L. supervised the project. Q.G. and C.K. wrote the manuscript. All authors have read and approved the manuscript.

Data availability

All relevant data can be found within the manuscript and its supplementary materials. The transcriptome reads have been submitted to the Sequence Read Archive at NCBI. The accession number is PRJNA997061.

Conflict of interest statement

The authors declare no competing interests.

References

[1]

Lin C . Blue light receptors and signal transduction. Plant Cell. 2002; 14: S207-25

[2]

Legris M, Ince YC, Fankhauser C . Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat Commun. 2019; 10: 5219

[3]

Rizzini L, Favory JJ, Cloix C, et al. Perception of UV-B by the Arabidopsis UVR8 protein. Science. 2011; 332: 103-6

[4]

Briggs WR, Rice HV . Phytochrome: chemical and physical properties and mechanism of action. Annu Rev Plant Physiol. 1972; 23: 293-334

[5]

Klose C, Viczian A, Kircher S, et al. Molecular mechanisms for mediating light-dependent nucleo/cytoplasmic partitioning of phytochrome photoreceptors. New Phytol. 2015; 206: 965-71

[6]

Zhao Y, Shi H, Pan Y, et al. Sensory circuitry controls cytosolic calcium-mediated phytochrome B phototransduction. Cell. 2023; 186: 1230-1243.e14

[7]

Sadanandom A, Ádám É, Orosa B, et al. SUMOylation of phytochrome-B negatively regulates light-induced signaling in Arabidopsis thaliana. Proc Natl Acad Sci. 2015; 112: 11108-13

[8]

Hahm J, Kim K, Qiu Y, et al. Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities. Nat Commun. 2020; 11: 1660

[9]

Legris M, Klose C, Burgie ES, et al. Phytochrome B integrates light and temperature signals in Arabidopsis. Science. 2016; 354: 897-900

[10]

Li FW, Melkonian M, Rothfels CJ, et al. Phytochrome diversity in green plants and the origin of canonical plant phytochromes. Nat Commun. 2015; 6: 7852

[11]

Clough RC, Vierstra RD . Phytochrome degradation. Plant Cell Environ. 1997; 20: 713-21

[12]

Duek PD, Fankhauser C . bHLH class transcription factors take centre stage in phytochrome signalling. Trends Plant Sci. 2005; 10: 51-4

[13]

Bae G, Choi G . Decoding of light signals by plant phytochromes and their interacting proteins. Annu Rev Plant Biol. 2008; 59: 281-311

[14]

Mao Z, He S, Xu F, et al. Photoexcited CRY1 and phyB interact directly with ARF6 and ARF8 to regulate their DNA-binding activity and auxin-induced hypocotyl elongation in Arabidopsis. New Phytol. 2020; 225: 848-65

[15]

Li K, Yu R, Fan LM, et al. DELLA-mediated PIF degradation contributes to coordination of light and gibberellin signalling in Arabidopsis. Nat Commun. 2016; 7: 11868

[16]

de Lucas M, Davière JM, Rodríguez-Falcón M, et al. A molecular framework for light and gibberellin control of cell elongation. Nature. 2008; 451: 480-4

[17]

Feng S, Martinez C, Gusmaroli G, et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature. 2008; 451: 475-9

[18]

Kim B, Jeong YJ, Corvalán C, et al. Darkness and gulliver2/phyB mutation decrease the abundance of phosphorylated BZR1 to activate brassinosteroid signaling in Arabidopsis. Plant J. 2014; 77: 737-47

[19]

Sweere U, Eichenberg K, Lohrmann J, et al. Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science. 2001; 294: 1108-11

[20]

Zhao Y, Sun J, Cherono S, et al. Colorful hues: insight into the mechanisms of anthocyanin pigmentation in fruit. Plant Physiol. 2023; 192: 1718-32

[21]

Holton TA, Cornish EC . Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell. 1995; 7: 1071-83

[22]

Tanaka Y, Ohmiya A . Seeing is believing: engineering anthocyanin and carotenoid biosynthetic pathways. Curr Opin Biotechnol. 2008; 19: 190-7

[23]

Zhao J, Dixon RA . The ’ins’ and ’outs’ of flavonoid transport. Trends Plant Sci. 2010; 15: 72-80

[24]

Xu W, Dubos C, Lepiniec L . Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci. 2015; 20: 176-85

[25]

An JP, Qu FJ, Yao JF, et al. The bZIP transcription factor MdHY5 regulates anthocyanin accumulation and nitrate assimilation in apple. Hortic Res. 2017; 4: 17023

[26]

Li YY, Mao K, Zhao C, et al. MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple. Plant Physiol. 2012; 160: 1011-22

[27]

Wang W, Wang P, Li X, et al. The transcription factor SlHY5 regulates the ripening of tomato fruit at both the transcriptional and translational levels. Hortic Res. 2021; 8: 83

[28]

Liu Y, Zhang XW, Liu X, et al. Phytochrome interacting factor MdPIF7 modulates anthocyanin biosynthesis and hypocotyl growth in apple. Plant Physiol. 2022; 188: 2342-63

[29]

Li Y, Xu P, Chen G, et al. FvbHLH9 functions as a positive regulator of anthocyanin biosynthesis by forming a HY5-bHLH9 transcription complex in strawberry fruits. Plant Cell Physiol. 2020; 61: 826-37

[30]

Liu Z, Liang T, Kang C . Molecular bases of strawberry fruit quality traits: advances, challenges, and opportunities. Plant Physiol. 2023; 193: 900-14

[31]

Denoyes B, Prohaska A, Petit J, et al. Deciphering the genetic architecture of fruit color in strawberry. J Exp Bot. 2023; 74: 6306-20

[32]

Lin-Wang K, Bolitho K, Grafton K, et al. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol. 2010; 10: 50

[33]

Lin-Wang K, McGhie TK, Wang M, et al. Engineering the anthocyanin regulatory complex of strawberry (Fragaria vesca). Front Plant Sci. 2014; 5: 651

[34]

Hawkins C, Caruana J, Schiksnis E, et al. Genome-scale DNA variant analysis and functional validation of a SNP underlying yellow fruit color in wild strawberry. Sci Rep. 2016; 6: 29017

[35]

Castillejo C, Waurich V, Wagner H, et al. Allelic variation of MYB10 is the major force controlling natural variation in skin and flesh color in strawberry (Fragaria spp.) fruit . The Plant Cell. 2020; 32: 3723-49

[36]

Luo X, Plunkert M, Teng Z, et al. Two MYB activators of anthocyanin biosynthesis exhibit specialized activities in petiole and fruit of diploid strawberry. J Exp Bot. 2023; 74: 1517-31

[37]

Yue M, Jiang L, Zhang N, et al. Regulation of flavonoids in strawberry fruits by FaMYB5/FaMYB10 dominated MYB-bHLH-WD40 ternary complexes. Front Plant Sci. 2023; 14: 1145670

[38]

Martinez-Rivas FJ, Blanco-Portales R, Serratosa MP, et al. FaMYB123 interacts with FabHLH3 to regulate the late steps of anthocyanin and flavonol biosynthesis during ripening. Plant J. 2023; 114: 683-98

[39]

Jiang L, Yue M, Liu Y, et al. A novel R2R3-MYB transcription factor FaMYB5 positively regulates anthocyanin and proanthocyanidin biosynthesis in cultivated strawberries (Fragaria x ananassa). Plant Biotechnol J. 2023; 21: 1140-58

[40]

Luo H, Dai C, Li Y, et al. Reduced Anthocyanins in petioles codes for a GST anthocyanin transporter that is essential for the foliage and fruit coloration in strawberry. J Exp Bot. 2018; 69: 2595-608

[41]

Gao Q, Luo H, Li Y, et al. Genetic modulation of RAP alters fruit coloration in both wild and cultivated strawberry. Plant Biotechnol J. 2020; 18: 1550-61

[42]

Clack T, Mathews S, Sharrock RA . The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Mol Biol. 1994; 25: 413-27

[43]

Yamaguchi R, Nakamura M, Mochizuki N, et al. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. J Cell Biol. 1999; 145: 437-45

[44]

Edger PP, VanBuren R, Colle M, et al. Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity . GigaScience. 2018; 7: 1-7

[45]

Xu H, Liu Q, Yao T, et al. Shedding light on integrative GA signaling. Curr Opin Plant Biol. 2014; 21: 89-95

[46]

Caruana JC, Sittmann JW, Wang W, et al. Suppressor of Runnerless encodes a DELLA protein that controls runner formation for asexual reproduction in strawberry. Mol Plant. 2018; 11: 230-3

[47]

Kang CY, Lian HL, Wang FF, et al. Cryptochromes, phytochromes, and COP1 regulate light-controlled stomatal development in Arabidopsis. Plant Cell. 2009; 21: 2624-41

[48]

Franklin KA, Quail PH . Phytochrome functions in Arabidopsis development. J Exp Bot. 2010; 61: 11-24

[49]

Dong H, Wang J, Song X, et al. HY5 functions as a systemic signal by integrating BRC1-dependent hormone signaling in tomato bud outgrowth. Proc Natl Acad Sci. 2023; 120: e2301879120

[50]

Jung JH, Domijan M, Klose C, et al. Phytochromes function as thermosensors in Arabidopsis. Science. 2016; 354: 886-9

[51]

Kircher S, Kozma-Bognar L, Kim L, et al. Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. Plant Cell. 1999; 11: 1445-56

[52]

Kadomura-Ishikawa Y, Miyawaki K, Noji S, et al. Phototropin 2 is involved in blue light-induced anthocyanin accumulation in Fragaria x ananassa fruits. J Plant Res. 2013; 126: 847-57

[53]

Liu Y, Tang L, Wang Y, et al. The blue light signal transduction module FaCRY1-FaCOP1-FaHY5 regulates anthocyanin accumulation in cultivated strawberry. Front Plant Sci. 2023; 14: 1144273

[54]

Xu P, Zawora C, Li Y, et al. Transcriptome sequencing reveals role of light in promoting anthocyanin accumulation of strawberry fruit. Plant Growth Regul. 2018; 86: 121-32

[55]

Kadomura-Ishikawa Y, Miyawaki K, Takahashi A, et al. Light and abscisic acid independently regulated FaMYB10 in Fragaria x ananassa fruit. Planta. 2015; 241: 953-65

[56]

Chen M, Chory J . Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol. 2011; 21: 664-71

[57]

Liu Z, Zhang Y, Wang J, et al. Phytochrome-interacting factors PIF4 and PIF5 negatively regulate anthocyanin biosynthesis under red light in Arabidopsis seedlings. Plant Sci. 2015; 238: 64-72

[58]

Bai S, Tao R, Yin L, et al. Two B-box proteins, PpBBX18 and PpBBX21, antagonistically regulate anthocyanin biosynthesis via competitive association with Pyrus pyrifolia ELONGATED HYPOCOTYL 5 in the peel of pear fruit . Plant J. 2019; 100: 1208-23

[59]

Bai S, Tao R, Tang Y, et al. BBX16, a B-box protein, positively regulates light-induced anthocyanin accumulation by activating MYB10 in red pear. Plant Biotechnol J. 2019; 17: 1985-97

[60]

Fang H, Dong Y, Yue X, et al. The B-box zinc finger protein MdBBX20 integrates anthocyanin accumulation in response to ultraviolet radiation and low temperature. Plant Cell Environ. 2019; 42: 2090-104

[61]

Bursch K, Toledo-Ortiz G, Pireyre M, et al. Identification of BBX proteins as rate-limiting cofactors of HY5. Nature Plants. 2020; 6: 921-8

[62]

de Wit M, Galvao VC, Fankhauser C . Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol. 2016; 67: 513-37

[63]

Liao X, Li M, Liu B, et al. Interlinked regulatory loops of ABA catabolism and biosynthesis coordinate fruit growth and ripening in woodland strawberry. Proc Natl Acad Sci U S A. 2018; 115: E11542-50

[64]

Zhou J, Sittmann J, Guo L, et al. Gibberellin and auxin signaling genes RGA1 and ARF8 repress accessory fruit initiation in diploid strawberry. Plant Physiol. 2021; 185: 1059-75

[65]

Devlin PF, Patel SR, Whitelam GC . Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell. 1998; 10: 1479-87

[66]

Ejaz M, Bencivenga S, Tavares R, et al. ARABIDOPSIS THALIANA HOMEOBOX GENE 1 controls plant architecture by locally restricting environmental responses. Proc Natl Acad Sci U S A. 2021; 118: e2018615118

[67]

Huang D, Wang S, Zhang B, et al. A gibberellin-mediated DELLA-NAC signaling cascade regulates cellulose synthesis in rice. Plant Cell. 2015; 27: 1681-96

[68]

McCarthy RL, Zhong R, Ye Z-H . MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell Physiol. 2009; 50: 1950-64

[69]

Zhong R, Richardson EA, Ye Z-H . Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta. 2007; 225: 1603-11

[70]

Zhong R, Ye Z-H . MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol. 2012; 53: 368-80

[71]

Li Y, Pi M, Gao Q, et al. Updated annotation of the wild strawberry Fragaria vesca V4 genome . Hort Res. 2019; 6: 61

[72]

Clough SJ, Bent AF . Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998; 16: 735-43

[73]

Feng J, Dai C, Luo H, et al. Reporter gene expression reveals precise auxin synthesis sites during fruit and root development in wild strawberry. J Exp Bot. 2019; 70: 563-74

[74]

Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013; 29: 15-21

[75]

Liao Y, Smyth GK, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014; 30: 923- 30

[76]

Love MI, Huber W, Anders S . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15: 550

[77]

Livak KJ, Schmittgen TD . Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001; 25: 402-8

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