Expansion and expression diversity of FAR1/FRS-like genes provides insights into flowering time regulation in roses

doi:10.1016/j.pld.2020.11.002

Abstract

Abstract: Roses are important horticultural plants with enormous diversity in flowers and flowering behavior. However, molecular regulation of flowering time variation in roses remains poorly characterized. Here, we report an expansion of the FAR1/FRS-like genes that correlates well with the switch to prostrate-toerect growth of shoots upon flowering in Rosa wichuraiana ‘Basye's Thornless’ (BT). With the availability of the high-quality chromosome-level genome assembly for BT that we developed recently, we identified 91 RwFAR1/FRS-like genes, a significant expansion in contrast to 52 in Rosa chinensis ‘Old Blush’ (OB), a founder genotype in modern rose domestication. Rose FAR1/FRS-like proteins feature distinct variation in protein domain structures. The dispersed expansion of RwFAR1/FRS-like genes occurred specifically in clade I and Ⅱ and is significantly associated with transposon insertion in BT. Most of the RwFAR1/FRS-like genes showed relatively higher expression level than their corresponding orthologs in OB. FAR1/FRS-like genes regulate light-signaling processes, shade avoidance, and flowering time in Arabidopsis thaliana. Therefore, the expansion and duplication of RwFAR1/FRS-like genes, followed by diversification in gene expression, might offer a novel leverage point for further understanding the molecular regulation of the variation in shoot-growth behavior and flowering time in roses.

Key words: Rose, FAR1/FRS-Like genes, Gene family expansion, Flowering time, Shoot growth behavior

Mi-Cai Zhong, Xiao-Dong Jiang, Wei-Hua Cui, Jin-Yong Hu. Expansion and expression diversity of FAR1/FRS-like genes provides insights into flowering time regulation in roses[J]. Plant Diversity, 2021, 43(02): 173-179.

References

Amasino, R.M., Michaels, S.D., 2010. The timing of flowering. Plant Physiol. 154, 516-520.
Andres, F., Coupland, G., 2012. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639.
Baurle, I., Dean, C., 2006. The timing of developmental transitions in plants. Cell 125, 655-664.
Bendahmane, M., Dubois, A., Raymond, O., et al., 2013. Genetics and genomics of flower initiation and development in roses. J. Exp. Bot. 64, 847-857.
Bulik-Sullivan, B.K., Loh, P.R., Finucane, H.K., et al., 2015. LD Score regression distinguishes confounding from polygenicity in genome-wide association studies.Nat. Genet. 47, 291-295.
Byrne, D.H., Anderson, N., Pemberton, H.B., 2007. The use of Rosa wichurana in the development of landscape roses adapted to hot humid climates. In:Pemberton, H.B. (Ed.), Proceedings of the Ivth International Symposium on Rose Research and Cultivation, vol. 1. Int Soc Horticultural Science, Leuven.
Cannon, S.B., Mitra, A., Baumgarten, A., et al., 2004. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 4, 10.
Chen, C., Chen, H., Zhang, Y., et al., 2020. TBtools:an integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 13, 1194-1202.
Crespel, L., Chirollet, M., Durel, C., et al., 2002. Mapping of qualitative and quantitative phenotypic traits in Rosa using AFLP markers. Theoret. Appl. Genetics. 105, 1207-1214.
Dodsworth, S., Chase, M.W., Leitch, A.R., 2016. Is post-polyploidization diploidization the key to the evolutionary success of angiosperms? Bot. J. Linn. Soc. 180, 1-5.
Dong, X., Jiang, X., Kuang, G., et al., 2017. Genetic control of flowering time in woody plants:roses as an emerging model. Plant Divers. 39, 104-110.
Emms, D.M., Kelly, S., 2019. OrthoFinder:phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238.
Flagel, L.E., Wendel, J.F., 2009. Gene duplication and evolutionary novelty in plants.New Phytol. 183, 557-564.
Fornara, F., de Montaigu, A., Coupland, G., 2010. SnapShot:control of flowering in Arabidopsis. Cell 141, 550, 550-1-e2.
Franklin, K.A., Whitelam, G.C., 2005. Phytochromes and shade-avoidance responses in plants. Ann. Bot. 96, 169-175.
Gao, Y., Liu, H., An, C., et al., 2013. Arabidopsis FRS4/CPD25 and FHY3/CPD45 work cooperatively to promote the expression of the chloroplast division gene ARC5 and chloroplast division. Plant J. 75, 795-807.
Grierson, C.S., Bames, S.R., Chase, M.W., et al., 2011. One hundred important questions facing plant science research. New Phytol. 192, 6-12.
Hibrand Saint-Oyant, L., Ruttink, T., Hamama, L., et al., 2018. A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nat. Plants. 4, 473-484.
Hu, B., Jin, J., Guo, A.Y., et al., 2015. GSDS 2.0:an upgraded gene feature visualization server. Bioinformatics 31, 1296-1297.
Hudson, M., Ringli, C., Boylan, M.T., et al., 1999. The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes Dev. 13, 2017-2027.
Iwata, H., Gaston, A., Remay, A., et al., 2012. The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J. 69, 116-125.
Johansson, M., Staiger, D., 2015. Time to flower:interplay between photoperiod and the circadian clock. J. Exp. Bot. 66, 719-730.
Katoh, K., Misawa, K., Kuma, K., et al., 2002. MAFFT:a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res. 30, 3059-3066.
Kim, D., Landmead, B., Salzberg, S.L., 2015. HISAT:a fast spliced aligner with low memory requirements. Nat. Methods 12, 357-360.
Li, D., Fu, X., Guo, L., et al., 2016. FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 113, 9375-9380.
Li, G., Siddiqui, H., Teng, Y., et al., 2011. Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis. Nat. Cell Biol. 13, 616-622.
Li, J.M., Qin, M.F., Qiao, X., et al., 2017. A new insight into the evolution and functional divergence of sweet transporters in Chinese white pear (Pyrus bretschneideri). Plant Cell Physiol. 58, 839-850.
Li, S., Yang, G., Yang, S., et al., 2019. The development of a high-density genetic map significantly improves the quality of reference genome assemblies for rose. Sci.Rep. 9, 5985.
Li, S., Zhong, M., Dong, X., et al., 2018. Comparative transcriptomics identifies patterns of selection in roses. BMC Plant Biol. 18, 371.
Li, S., Zhou, N., Zhou, Q., et al., 2015. Inheritance of perpetual blooming in Rosa chinensis ‘Old Blush’. Hortic. Plant J. 1, 108-112.
Lin, R., Ding, L., Casola, C., et al., 2007. Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318, 1302-1305.
Lin, R., Wang, H., 2004. Arabidopsis FHY3/FAR1 gene family and distinct roles of its members in light control of Arabidopsis development. Plant Physiol. 136, 4010-4022.
Liu, Y., Ma, M., Li, G., et al., 2020. Transcription factors FHY3 and FAR1 regulate lightinduced CIRCADIAN CLOCK ASSOCIATED1 gene expression in Arabidopsis. Plant Cell 32, 1464-1478.
Liu, Y., Wei, H., Ma, M., et al., 2019. Arabidopsis FHY3 and FAR1 regulate the balance between growth and defense responses under shade conditions. Plant Cell 31, 2089-2106.
Liu, Y., Xie, Y., Wang, H., et al., 2017. Light and ethylene coordinately regulate the phosphate starvation response through transcriptional regulation of PHOSPHATE STARVATION RESPONSE1. Plant Cell 29, 2269-2284.
Ma, L., Li, G., 2018. FAR1-RELATED SEQUENCE (FRS) and FRS-RELATED FACTOR (FRF) family proteins in Arabidopsis growth and development. Front. Plant Sci. 9, 692.
Ma, L., Tian, T., Lin, R., et al., 2016. Arabidopsis FHY3 and FAR1 regulate light-induced myo-inositol biosynthesis and oxidative stress responses by transcriptional activation of MIPS1. Mol. Plant 9, 541-557.
Ma, L., Xue, N., Fu, X., et al., 2017. Arabidopsis thaliana FAR-RED ELONGATED HYPOCOTYLS3 (FHY3) and FAR-RED-IMPAIRED RESPONSE1 (FAR1) modulate starch synthesis in response to light and sugar. New Phytol. 213, 1682-1696.
McCormac, A.C., Terry, M.J., 2002. Light-signalling pathways leading to the coordinated expression of HEMA1 and Lhcb during chloroplast development in Arabidopsis thaliana. Plant J. 32, 549-559.
Munnik, T., Nielsen, E., 2011. Green light for polyphosphoinositide signals in plants.Curr. Opin. Plant Biol. 14, 489-497.
O'Malley, R.C., Huang, S.S.C., Song, L., et al., 2016. Cistrome and epicistrome features shape the regulatory DNA landscape. Cell 165, 1280-1292.
Ouyang, X., Li, J., Li, G., et al., 2011. Genome-wide binding site analysis of FAR-RED ELONGATED HYPOCOTYL3 reveals its novel function in Arabidopsis development. Plant Cell 23, 2514-2535.
Panchy, N., Lehti-Shiu, M., Shiu, S.H., 2016. Evolution of gene duplication in plants.Plant Physiol. 171, 2294-2316.
Pennisi, Elizabeth, 2005. What determins species diversity? Science 309, 90.
Pertea, M., Pertea, G.M., Antonescu, C.M., et al., 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290-295.
Qiao, X., Li, Q.H., Yin, H., et al., 2019. Gene duplication and evolution in recurring polyploidization-diploidization cycles in plants. Genome Biol. 20, 38.
Randoux, M., Daviere, J.M., Jeauffre, J., et al., 2014. RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose. New Phytol. 202, 161-173.
Randoux, M., Jeauffre, J., Thouroude, T., et al., 2012. Gibberellins regulate the transcription of the continuous flowering regulator, RoKSN, a rose TFL1 homologue.J. Exp. Bot. 63, 6543-6554.
Raymond, O., Gouzy, J., Just, J., et al., 2018. The Rosa genome provides new insights into the domestication of modern roses. Nat. Genet. 50, 772-777.
Ritter, A., Iñigo, S., Fernández-Calvo, P., et al., 2017. The transcriptional repressor complex FRS7-FRS12 regulates flowering time and growth in Arabidopsis. Nat.Commun. 8, 15235.
Saha, S., Bridges, S., Magbanua, Z.V., Peterson, D.G., 2008. Empirical comparision of ab initio repeat finding programs. Nucleic Acids Res. 36, 2284-2294.
Shupert, D.A., Byme, D.H., Pemberton, H.B., 2007. Inheritance of flower traits, leaflet number and prickles in roses. In:Pemberton, H.B. (Ed.), Proceedings of the Ivth International Symposium on Rose Research and Cultivation, vol. 1. Int Soc Horticultural Science, Leuven.
Siddiqui, H., Khan, S., Rhodes, B.M., et al., 2016. FHY3 and FAR1 act downstream of light stable phytochromes. Front. Plant Sci. 7, 175.
Spiller, M., Linde, M., Hibrand-Saint Oyant, L., et al., 2011. Towards a unified genetic map for diploid roses. Theoret. Appl. Genetics. 122, 489-500.
Stamatakis, A., 2014. RAxML version 8:a tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics 30, 1312-1313.
Sun, Y.B., Zhang, X.J., Zhong, M.C., et al., 2020. Genome-wide identification of WD40 genes reveals a functional diversification of COP1-like genes in Rosaceae. Plant Mol. Biol. 104, 81-95.
Tang, W., Ji, Q., Huang, Y., et al., 2013. FAR-RED ELONGATED HYPOCOTYl3 and FARRED IMPAIRED RESPONSE1 transcription factors integrate light and abscisic acid signaling in Arabidopsis. Plant Physiol. 163, 857-866.
Tang, W., Wang, W., Chen, D., et al., 2012. Transposase-derived proteins FHY3/FAR1 interact with PHYTOCHROME-INTERACTING FACTOR1 to regulate chlorophyll biosynthesis by modulating HEMB1 during deetiolation in Arabidopsis. Plant Cell 24, 1984-2000.
Wang, W., Tang, W., Ma, T., et al., 2016. A pair of light signaling factors FHY3 and FAR1 regulates plant immunity by modulating chlorophyll biosynthesis.J. Integr. Plant Biol. 58, 91-103.
Wang, Y.P., Tang, H.B., DeBarry, J.D., et al., 2012. MCScanX:a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49.
Xie, Y., Zhou, Q., Zhao, Y., et al., 2020. FHY3 and FAR1 integrate light signals with the miR156-SPL module-mediated aging pathway to regulate Arabidopsis flowering.Mol. Plant 13, 483-498.
Zhang, R., Yang, C., Jiang, Y., et al., 2019. A PIF7-CONSTANS-Centered molecular regulatory network underlying shade-accelerated flowering. Mol. Plant 12, 1587-1597.
Zheng, Y., Jiao, C., Sun, H.H., et al., 2016. iTAK:a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol. Plant 9, 1667-1670.
Zhong, M.-C., Jiang, X.-D., Yang, G.-Q., et al., 2020. Genomic hitchhiking with moisture adaptation patterns stem prickleless in rose. bioRxiv. https://doi.org/10.1101/2020.07.16.207795.

[1]	Fei-Hong Yan, Li-Ping Zhang, Fang Cheng, Dong-Mei Yu, Jin-Yong Hu. Accession-specific flowering time variation in response to nitrate fluctuation in Arabidopsis thaliana [J]. Plant Diversity, 2021, 43(01): 78-85.
[2]	Lei Xiang, Yanmei Li, Xiaolin Sui, Airong Li. Fast and abundant in vitro spontaneous haustorium formation in root hemiparasitic plant Pedicularis kansuensis Maxim. (Orobanchaceae) [J]. Plant Diversity, 2018, 40(05): 226-231.
[3]	Yuanyuan Liu, Xin Yin, Ya Yang, Chuntao Wang, Yongping Yang. Molecular cloning and expression analysis of turnip (Brassica rapa var. rapa) sucrose transporter gene family [J]. Plant Diversity, 2017, 39(03): 123-129.
[4]	Xue Dong, Xiaodong Jiang, Guoqiang Kuang, Qingbo Wang, Micai Zhong, Dongmin Jin, Jinyong Hu. Genetic control of flowering time in woody plants: Roses as an emerging model [J]. Plant Diversity, 2017, 39(02): 104-110.
[5]	WANG Yi, QUAN Qiu-Mei, LI Yun-Xiang. Effects of Flowering Period on Nectar Secretion and Fruit Set of Epimedium wushanense (Berberidaceae) [J]. Plant Diversity, 2012, 34(5): 471-477.
[6]	LI Shu-Fa , ZHANG Hao , TANG Kai-Xue, WANG Qi-Gang , WANG Zhong-You. Photosynthetic Characteristics of Cut Roses under Greenhouse Condition in the Middle of Yunnan Province [J]. Plant Diversity, 2008, 30(01): 99-104.
[7]	ZHANG Shi-Bao, HU Hong, LI Shu-Yun. Advances in Genetic Engineering of the Flowers and Plants II: Flower Shape, Flowering Time and Shelf Life of Flower [J]. Plant Diversity, 2002, 24(01): 1-3.
[8]	HOU Xue - Wen GUO Yong. The Found of a New Method to Rapidly Measure Biomass of Suspension Plant Cell Culture [J]. Plant Diversity, 2001, 23(04): 1-3.
[9]	HU Xiao-Bin YANG Pei-Quan LIU Wei-Jian. A NEW INDANONE ISOLATED FROM DROSERA PELTATA VAR. LUNATA [J]. Plant Diversity, 1991, 13(03): 1-3.
[10]	Jin Qiduan, Zhou Qianlan, Mu Quanzhang. STRUCTURE OF DREGEOSIDE A FROM DREGEA SINENSIS VAR. CORRUGATA [J]. Plant Diversity, 1988, 10(04): 1-3.