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Research paper

Species-specific regulatory pathways of small RNAs play sophisticated roles in flower development in Dimocarpus longan Lour.

Bo Liua,b,cGuanliang Lia,b,cChengjie Chena,b,cZaohai Zenga,b,cJing Xua,b,cJisen ZhangdRui Xiaa,b,c( )Yuanlong Liua,b,c( )
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, Guangdong 510640, China
Guangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, Guangdong 510640, China
Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in South China, Ministry of Agriculture and Rural Affairs, South China Agricultural University, Guangzhou, Guangdong 510640, China
Center for Genomics and Biotechnology, Haixia Institute of Science and Technology, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, China

Peer review under responsibility of Chinese Society of Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS)

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Abstract

Flower development plays vital role in horticultural plants. Post-transcriptional regulation via small RNAs is important for plant flower development. To uncover post-transcriptional regulatory networks during the flower development in Dimocarpus longan Lour. ‘Shixia’, an economically important fruit crop in subtropical regions, we collected and analyzed sRNA deep-sequencing datasets and degradome libraries Apart from identifying miRNAs and phased siRNA generating loci (PHAS loci), 120 hairpin loci, producing abundant sRNAs, were identified by in-house protocols. Our results suggested that 56 miRNA-target pairs, 2221-nt-PHAS loci, and 111 hairpin loci are involved in post-transcriptional gene silencing during longan reproductive development. Lineage-specific or species-specific post-transcriptional regulatory modules have been unveiled, including miR482-PHAS and miRN15. miR482-PHAS might be involved in longan flower development beyond their conserved roles in plant defense, and miRN15 is a novel miRNA likely associated with a hairpin locus (HPL-056) to regulate strigolactone receptor gene DWARF14 (D14) and the biogenesis of phasiRNAs from D14. These small RNAs are enriched in flower buds, suggesting they are likely involved in post-transcriptional regulatory networks essential for longan flower development via the strigolactone signaling pathway.

References

 

Achkar, N.P., Cambiagno, D.A., Manavella, P.A., 2016. miRNA Biogenesis: A Dynamic Pathway. Trends Plant Sci, 21: 1034-1044.

 

Arite, T., Umehara, M., Ishikawa, S., Hanada, A., Maekawa, M., Yamaguchi, S., Kyozuka, J., 2009. D14, a strigolactone-Insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol, 50: 1416-1424.

 

Axtell, M.J., Meyers, B.C., 2018. Revisiting criteria for plant microRNA annotation in the Era of big data. Plant Cell, 30: 272-284.

 

Borges, F., Martienssen, R.A., 2015. The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol, 16: 727-741.

 

Braun, N., de Saint Germain, A., Pillot, J.-P., Boutet-Mercey, S., Dalmais, M., Antoniadi, I., Li, X., Maia-Grondard, A., Le Signor, C., Bouteiller, N., 2012. The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol, 158: 225-238.

 

Brousse, C., Liu, Q., Beauclair, L., Deremetz, A., Axtell, M.J., Bouche, N., 2014. A non-canonical plant microRNA target site. Nucleic Acids Res, 42: 5270-5279.

 

Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., Madden, T.L., 2009. BLAST+: Architecture and applications. BMC Bioinf, 10: 1-9.

 

Chavez Montes, R.A., De Fatima Rosas-Cardenas, F., De Paoli, E., Accerbi, M., Rymarquis, L.A., Mahalingam, G., Marsch-Martinez, N., Meyers, B.C., Green, P.J., De Folter, S., 2014. Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat Commun, 5: 1-15.

 

Chen, C., Chen, H., Zhang, Y., Thomas, H.R., Frank, M.H., He, Y., Xia, R., 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 13: 1194-1202.

 

Chen, C., Li, J., Feng, J., Liu, B., Feng, L., Yu, X., Li, G., Zhai, J., Meyers, B.C., Xia, R., 2021. sRNAanno—a database repository of uniformly annotated small RNAs in plants. Hortic Res, 8: 45.

 

Chen, X.M., Shi, X.Y., Ai, Q., Han, J.Y., Wang, H.S., Fu, Q.S., 2022. Transcriptomic and metabolomic analyses reveal that exogenous strigolactones alleviate the response of melon root to cadmium stress. Hortic Plant J, 8: 637-649.

 

Cho, S.H., Coruh, C., Axtell, M.J., 2013. miR156 and miR390 regulate tasiRNA accumulation and developmental timing in physcomitrella patens. Plant Cell, 24: 4837-4849.

 

Feng, L., Xia, R., Liu, Y., 2019. Comprehensive characterization of miRNA and PHAS loci in the diploid strawberry (Fragaria vesca) genome. Hortic Plant J, 5: 255-267.

 

Gao, X.Q., Wang, N., Wang, X.L., Zhang, X.S., 2019. Architecture of wheat inflorescence: insights from rice. Trends Plant Sci, 24: 802-809.

 

Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Pages, V., Dun, E.A., Pillot, J.P., Letisse, F., Matusova, R., Danoun, S., Portais, J.C., Bouwmeester, H., Becard, G., Beveridge, C.A., Rameau, C., Rochange, S.F., 2008. Strigolactone inhibition of shoot branching. Nature, 455: 189-194.

 

Hamiaux, C., Drummond, R.S.M., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D., Snowden, K.C., 2012. DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol, 22: 2032-2036.

 

Huang, S., Han, D., Wang, J., Guo, D., Li, J., 2021. Floral induction of longan (Dimocarpus longan) by Potassium chlorate: application, mechanism, and future perspectives. Front Plant Sci, 12: 1-8.

 

Jia, T., Wei, D., Meng, S., Allan, A.C., Zeng, L., 2014. Identification of regulatory genes implicated in continuous flowering of longan (Dimocarpus longan L.). PLoS One, 9: 1-24.

 

Jiang, P., Lian, B., Liu, C., Fu, Z., Shen, Y., Cheng, Z., Qi, Y., 2020. 21-nt phasiRNAs direct target mRNA cleavage in rice male germ cells. Nat Commun, 11: 5191.

 

Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., Dong, G., Zeng, D., Lu, Z., Zhu, X., Qian, Q., Li, J., 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet, 42: 541-544.

 

Jue, D., Sang, X., Liu, L., Shu, B., Wang, Yicheng, Liu, C., Wang, Yi, Xie, J., Shi, S., 2019. Comprehensive analysis of the longan transcriptome reveals distinct regulatory programs during the floral transition. BMC Genom, 20: 126.

 

Kalvari, I., Nawrocki, E.P., Argasinska, J., Quinones-Olvera, N., Finn, R.D., Bateman, A., Petrov, A.I., 2018. Non-Coding RNA analysis using the Rfam Database. Curr Protoc Bioinforma, 62: 1-27.

 

Kaplan, B., Sherman, T., Fromm, H., 2007. Cyclic nucleotide-gated channels in plants. FEBS Lett, 581: 2237-2246.

 

Kohlen, W., Charnikhova, T., Lammers, M., Pollina, T., Toth, P., Haider, I., Pozo, M.J., de Maagd, R.A., Ruyter-Spira, C., Bouwmeester, H.J., 2012. The tomato CAROTENOID CLEAVAGE DIOXYGENASE 8 (SlCCD 8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol, 196: 535-547.

 

Komiya, R., Ohyanagi, H., Niihama, M., Watanabe, T., Nakano, M., Kurata, N., Nonomura, K.I., 2014. Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J, 78: 385-397.

 

Langmead, B., 2010. Aligning short sequencing reads with Bowtie. Curr Protoc Bioinforma, 32: 11.7.1-11.7.14.

 

Lee, Y.C., Chang, J.C., 2019. Leafless inflorescence produces more female flowers and fruit yield than leafy inflorescence in ‘yu her pau’ litchi. Hort Science, 54: 487-491.

 

Li, P., Su, T., Zhang, D., Wang, W., Xin, X., Yu, Y., Zhao, X., Yu, S., Zhang, F., 2021. Genome-wide analysis of changes in miRNA and target gene expression reveals key roles in heterosis for Chinese cabbage biomass. Hortic Res, 8: 1-15.

 

Li, Y., Meng, X.W., Ma, Z.H., Liu, M.J., Zhao J., 2022. Identification and expression analysis of microRNA families associated with phase transition in Chinese jujube. Acta Hortic Sin, 49: 23-40. (in Chinese)

 

Liu, Y., Teng, C., Xia, R., Meyers, B.C., 2020. PhasiRNAs in Plants: Their Biogenesis, genic sources, and roles in stress responses, development, and reproduction. Plant Cell, 32: 3059-3080.

 

Mallory, A., Vaucheret, H., 2010. Form, function, and regulation of ARGONAUTE proteins. Plant Cell, 22: 3879-3889.

 

Mano, S., Nakamura, T., Kondo, M., Miwa, T., Nishikawa, S.I., Mimura, T., Nagatani, A., Nishimura, M., 2014. The plant organelles database 3 (PODB3) update 2014: Integrating electron micrographs and new options for plant organelle research. Plant Cell Physiol, 55: 1-9.

 

Miura, K., Ikeda, M., Matsubara, A., Song, X.J., Ito, M., Asano, K., Matsuoka, M., Kitano, H., Ashikari, M., 2010. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet, 42: 545-549.

 

Pokhrel, S., Huang, K., Belanger, S., Zhan, J., Caplan, J.L., Kramer, E.M., Meyers, B.C., 2021. Pre-meiotic 21-nucleotide reproductive phasiRNAs emerged in seed plants and diversified in flowering plants. Nat Commun, 12: 4941.

 

Seto, Y., Yasui, R., Kameoka, H., Tamiru, M., Cao, M., Terauchi, R., Sakurada, A., Hirano, R., Kisugi, T., Hanada, A., Umehara, M., Seo, E., Akiyama, K., Burke, J., Takeda-Kamiya, N., Li, W., Hirano, Y., Hakoshima, T., Mashiguchi, K., Noel, J.P., Kyozuka, J., Yamaguchi, S., 2019. Strigolactone perception and deactivation by a hydrolase receptor DWARF14. Nat Commun, 10: 191.

 

Shahid, S., Kim, G., Johnson, N.R., Wafula, E., Wang, F., Coruh, C., Bernal-Galeano, V., Phifer, T., Depamphilis, C.W., Westwood, J.H., Axtell, M.J., 2018. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature, 553: 82-85.

 

Sharma, A., Badola, P.K., Bhatia, C., Sharma, D., Trivedi, P.K., 2020. Primary transcript of miR858 encodes regulatory peptide and controls flavonoid biosynthesis and development in Arabidopsis. Nat Plants, 6: 1262-1274.

 

Shuai, P., Su, Y., Liang, D., Zhang, Z., Xia, X., Yin, W., 2016. Identification of phasiRNAs and their drought-responsiveness in Populus trichocarpa. FEBS Lett, 590: 3616-3627.

 

Song, X., Lu, Z., Yu, H., Shao, G., Xiong, J., Meng, X., Jing, Y., Liu, G., Xiong, G., Duan, J., Yao, X.F., Liu, C.M., Li, H., Wang, Y., Li, J., 2017. IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res, 27: 1128-1141.

 

Sun, Q., Liu, X., Yang, J., Liu, W., Du, Q., Wang, H., Fu, C., Li, W.X., 2018. MicroRNA528 affects lodging resistance of maize by regulating lignin biosynthesis under nitrogen-luxury conditions. Mol Plant, 11: 806-814.

 

Sun, Q., Xie, Y., Li, H., Liu, J., Geng, R., Wang, P., Chu, Z., Chang, Y., Li, G., Zhang, X., 2021. Cotton GhBRC1 regulates branching, flowering, and growth by integrating multiple hormone pathways. Crop J, 10: 75-87.

 

Thimmappa, R., Geisler, K., Louveau, T., O’Maille, P., Osbourn, A., 2014. Triterpene biosynthesis in plants. Annu Rev Plant Biol, 65: 225-257.

 

Wang, B., Tan, H.W., Fang, W., Meinhardt, L.W., Mischke, S., Matsumoto, T., Zhang, D., 2015. Developing single nucleotide polymorphism (SNP) markers from transcriptome sequences for identification of longan (Dimocarpus longan) germplasm. Hortic Res, 2: 1-10.

 

Wang, J.W., Czech, B., Weigel, D., 2009. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell, 138: 738-749.

 

Wang, L., Wang, B., Yu, H., Guo, H., Lin, T., Kou, L., Wang, A., Shao, N., Ma, H., Xiong, G., Li, X., Yang, J., Chu, J., Li, J., 2020. Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature, 583: 277-281.

 

Wu, G., Park, M.Y., Conway, S.R., Wang, J.W., Weigel, D., Poethig, R.S., 2009. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell, 138: 750-759.

 

Xia, R., Chen, C., Pokhrel, S., Ma, W., Huang, K., Patel, P., Wang, F., Xu, J., Liu, Z., Li, J., Meyers, B.C., 2019. 24-nt reproductive phasiRNAs are broadly present in angiosperms. Nat Commun, 10: 1-8.

 

Xia, R., Meyers, B.C., Liu, Zhongchi, Beers, E.P., Ye, S., Liu, Zongrang, 2013. MicroRNA superfamilies descended from miR390 and their roles in secondary small interfering RNA biogenesis in eudicots. Plant Cell, 25: 1555-1572.

 

Xia, R., Xu, J., Meyers, B.C., 2017. The emergence, evolution, and diversification of the miR390-TAS3-ARF pathway in land plants. Plant Cell, 29: 1232-1247.

 

Xia, R., Ye, S., Liu, Z.R., Meyers, B.C., Liu, Z.C., 2015. Novel and recently evolved microRNA clusters regulate expansive F-BOX gene networks through phased small interfering RNAs in wild diploid strawberry. Plant Physiol, 169: 594-610.

 

Xie, Y., Liu, Y., Ma, M., Zhou, Q., Zhao, Y., Zhao, B., Wang, B., Wei, H., Wang, H., 2020. Arabidopsis FHY3 and FAR1 integrate light and strigolactone signaling to regulate branching. Nat Commun, 11: 1-13.

 

Yang, R., Li, P., Mei, H., Wang, D., Sun, J., Yang, C., Hao, L., Cao, S., Chu, C., Hu, S., Song, X., Cao, X., 2019. Fine-tuning of MiR528 accumulation modulates flowering time in rice. Mol Plant, 12: 1103-1113.

 

Yao, R., Ming, Z., Yan, L., Li, S., Wang, F., Ma, S., Yu, C., Yang, M., Chen, Li, Chen, L.H., Li, Y., Yan, C., Miao, D., Sun, Z., Yan, J., Sun, Y., Wang, L., Chu, J., Fan, S., He, W., Deng, H., Nan, F., Li, J., Rao, Z., Lou, Z., Xie, D., 2016. DWARF14 is a non-canonical hormone receptor for strigolactone. Nature, 536: 469-473.

 

Yao, S., Yang, Z., Yang, R., Huang, Y., Guo, G., Kong, X., Lan, Y., Zhou, T., Wang, H., Wang, W., Cao, X., Wu, J., Li, Y., 2019. Transcriptional regulation of miR528 by OsSPL9 orchestrates antiviral response in rice. Mol Plant, 12: 1114-1122.

 

Zhai, J., Jeong, D.H., de Paoli, E., Park, S., Rosen, B.D., Li, Y., Gonzalez, A.J., Yan, Z., Kitto, S.L., Grusak, M.A., Jackson, S.A., Stacey, G., Cook, D.R., Green, P.J., Sherrier, D.J., Meyers, B.C., 2011. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev, 25: 2540-2553.

 

Zhang, L.B., Xia H., Wu J.S., Li M.T., 2022a. MiRNA identification, characterization and integrated network analysis for flavonoid biosynthesis in Brassicacoraphanus. Hortic Plant J, 8: 319-327.

 

Zhang, Q., Ma, C., Zhang, Y., Gu, Z., Li, W., Duan, X., Wang, Shengnan, Hao, L., Wang, Y., Wang, Shengyuan, Li, T., 2018. A single-nucleotide polymorphism in the promoter of a hairpin rna contributes to alternaria alternata leaf spot resistance in apple (Malus × domestica). Plant Cell, 30: 1924-1942.

 

Zhang, Q.W., Yang, X., Li, F., Deng, Y.T., 2022b. Advances in miRNA-mediated growth and development regulation in horticultural crops. Acta Hortic Sin, 49: 1145-1161. (in Chinese)

 

Zhang, Y., Waseem, M., Zeng, Z., Xu, J., Chen, C., Liu, Y., Zhai, J., Xia, R., 2021. MicroRNA482/2118, a miRNA superfamily essential for both disease resistance and plant development. New Phytol, 233: 2047-2057.

 

Zhu, H., Chen, C., Zeng, J., Yun, Z., Liu, Y., Qu, H., Jiang, Y., Duan, X., Xia, R., 2020. MicroRNA528, a hub regulator modulating ROS homeostasis via targeting of a diverse set of genes encoding copper-containing proteins in monocots. New Phytol, 225: 385-399.

Horticultural Plant Journal
Pages 237-249
Cite this article:
Liu B, Li G, Chen C, et al. Species-specific regulatory pathways of small RNAs play sophisticated roles in flower development in Dimocarpus longan Lour.. Horticultural Plant Journal, 2023, 9(2): 237-249. https://doi.org/10.1016/j.hpj.2022.12.004

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Received: 03 May 2022
Revised: 17 July 2022
Accepted: 10 October 2022
Published: 21 December 2022
© 2022 Chinese Society for Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS).

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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