Manipulating osa-MIR156f Expression by D18 Promoter to Regulate Plant Architecture and Yield Traits both in Seasonal and Ratooning Rice

Liu et al. Biological Procedures Online (2019) 21:21 https://doi.org/10.1186/s12575-019-0110-4 RESEARCH Open Access Manipulating osa-MIR156f Expression by D18 Promoter to Regulate Plant Architecture and Yield Traits both in Seasonal and Ratooning Rice Qing Liu1†, Yi Su1,2†, Yunhua Zhu3, Keqin Peng1, Bin Hong1, Ruozhong Wang1,2, Mahmoud Gaballah4 and Langtao Xiao1,2* Abstract Background: Rice (Oryza sativa L.) feeds more than half of the world’s population. Ratooning rice is an economical alternative to the second seasonal rice, thus increasing the yield of ratooning rice is highly important. Results: Here we report an applicable transgenic line constructed through the manipulation of osa-MIR156f expression in rice shoot using the OsGA3ox2 (D18) promoter. In seasonal rice, the D18–11 transgenic line showed moderate height and more effective tillers with normal panicle. In ratooning rice, axillary buds outgrew from the basal node of the D18–11 transgenic line before the harvest of seasonal rice. More effective tillers produced by the outgrowth of axillary buds contributed to the plant architecture improvement and yield increase. Additionally, it was found that osa-miR156f down-regulated the expression of tillering regulators, such as TEOSINTE BRANCHED1 (TB1) and LAX PANICLE 1 (LAX1). The expression of DWARF10, DWARF27 and DWARF53, three genes being involved in the biosynthesis and signaling of strigolactone (SL), decreased in the stem of the D18–11 transgenic line. Conclusion: Our results indicated that the manipulation of osa-MIR156f expression may have application significance in rice genetic breeding. This study developed a novel strategy to regulate plant architecture and grain yield potential both in the seasonal and ratooning rice. Keywords: Seasonal rice, Ratooning rice, Osa-MIR156f, Plant architecture, Grain yield Background Rice (Oryza sativa L.) is the staple food of more than half of the world’s population which is expected to reach 9 billion by the year of 2050. To meet the needs of the projected population, at least a 40% improvement of crop yield will be needed by 2025 [1, 2]. Therefore, increasing crop yield is one of the most important goals in modern agriculture. The ideal plant architecture for rice, i.e. the phenotype of moderate height, enough effective tillers, large panicle and robust stems/roots, is crucial for high yield [3, 4]. In the * Correspondence: † Qing Liu and Yi Su contributed equally to this work. 1 Hunan Provincial Key Laboratory of Phytohormones and Growth Development, Hunan Agricultural University, Changsha 410128, China 2 Southern Regional Collaborative Innovation Center for Grain and Oil Crops in China, Hunan Agricultural University, Changsha 410128, China Full list of author information is available at the end of the article past two decades, various genes regulating rice plant architecture related traits have been identified. For example, Grain number 1a (Gn1a) [5] and ABERRANT PANICLE ORGANIZATION 1 (APO1) [6] regulate grain number. Grain Size 3 (GS3), Grain Weight 2 (GW2) and SQUAMOSA-PROMOTER BINDING LIKE 13 (SPL13) regulate grain size [7–10]. DENSE AND ERECT PANICLE 1 (DEP1), SMALL PANICLE (SPA) and LAX PANICLE 1 (LAX1) control panicle size [11, 12]. SPL14 promotes panicle branching and grain yield [13, 14]. TEOSINTE BRANCHED1 (TB1) regulates lateral branching and represses the outgrowth of axillary buds [15]. MONOCULM 1 (MOC1) controls rice branching and axillary meristem initiation [16]. ELONGATED UPPERMOST INTERNODE1 (EUI1), SEMI DWARF1 (SD1), SLENDER RICE1 (SLR1), GA-INSENSITIVE DWARF1 (GID1) and GID2, several © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Liu et al. Biological Procedures Online (2019) 21:21 genes being related to gibberellin (GA) biosynthesis/signaltransduction, jointly regulate plant height [17]. The successful identification of these genes involved in rice plant architecture regulation greatly promoted the elucidation of the underlying molecular mechanisms. Strigolactones (SLs) regulate rice tiller development through interactions with tillering related genes. DWARF 53 (D53), the repressor of the SL signaling pathway, is able to directly interact with the N-terminal domains of miR156-controlled SPLs and represses the expression of TB1 [13, 18, 19]. SPL14 interacts with MADS57, which directly binds to the CArG motif of the DWARF14 (D14) promoter and suppresses D14 transcription to control the outgrowth of axillary buds in rice [20]. LAX1 and Rice Leafy Homolog1 (RFL), being highly co-expressed with SPL7, SPL14, and SPL17, are down-regulated in the panicles of the osa-MIR156 overexpression line [11, 21, 22]. SPL14 is able to bind to the LAX1 promoter, which implies that LAX1 may also be directly regulated by SPL14 [23]. The expression of Rice TFL1/CEN homolog1 (RCN1) is suppressed by MADS34 [24, 25]. MADS34, SPL, LAX1 and RFL are down-regulated in the osa-MIR156b and osaMIR156h overexpression line [26]. Several studies focused on the important regulators for rice plant architecture. Among them, microRNAs show immense application potential in genetic breeding because of their flexible and precise regulation of tillering and panicle branching. miR156 targets SPLs and regulates plant growth and development [27]. Furthermore, miR156 and SPLs are involved in plant embryogenesis [28], shoot maturation [29], flowering control [30], phase change [27, 31– 34], biomass production [31, 35], panicle cell death [36], and crown root development [37]. In rice, ten osa-MIR156 genes produce five mature osa-miR156 sequences and the overexpression of osa-MIR156 produces more tillers [26]. SPL14 defines the plant architecture by decreasing tiller number and increasing plant height/panicle branch number, thus shows great potential for genetic breeding [13, 14]. Interestingly, SPL14 mRNA contains a recognition site for miR156 and its spatiotemporal expression is strictly controlled by miR156. Our previous study also found that a high level of osa-MIR156f in rice caused a dwarf and multi-tillering phenotype [38]. Additional regulatory networks, such as the miR529/SPL, miR172/AP2 and miR156/miR159 pathways, also influence rice tillering and panicle branching [23, 34, 39]. Moreover, SLs suppress shoot branching by inhibiting the outgrowth of axillary buds through the D53 repressor signaling pathway. D53 interacts with IDEAL PLANT ARCHITECTURE1 (IPA1) in vivo and in (...truncated)