Differential expression of miRNA and function of target genes in heteromorphic leaves of Populus euphratica
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摘要:目的异形叶性是植物为适应环境在同一植株上产生多种形态成熟叶片的现象。胡杨是典型的木本异形叶植物，前人研究发现，胡杨异形叶片间展现出不同的生理特性及环境适应性。本研究拟通过对胡杨异形叶差异表达miRNA及其靶基因功能的分析，揭示胡杨叶片形态及其生理变化的分子调控机制。方法以成年胡杨披针形叶和锯齿卵圆形叶为实验材料，通过高通量测序对其miRNA的表达模式及差异表达miRNA的靶基因功能进行比较研究。结果共获得6个高质量的sRNA文库，各文库有效序列占原始序列的56% ~ 81%。通过比对，共鉴定517个已知miRNA和127个新预测miRNA，主要长度分布区间为20 ~ 22 nt，其中的389个miRNA匹配至54个已知的miRNA家族。两种形态叶片共同检出的miRNA有369个，与披针形叶片相比，锯齿卵圆形叶中7个miRNA上调表达，15个下调表达。通过靶基因预测及功能分析，发现差异表达miRNA参与调控胡杨异形叶的抗逆相关途径，如对盐胁迫的响应，磷酸肌醇代谢，角质、软木脂和蜡的生物合成，碱基切除修复和RNA降解等代谢途径。利用实时荧光定量PCR验证了5个差异表达miRNA的表达趋势与高通量测序结果一致，通过PCR检测发现差异表达miRNA与其靶基因存在一定的负调控关系。结论胡杨异形叶中miRNA表达模式存在差异。其中，调控植物生长发育的保守的miR167、miR166及调控植物抗逆性的miR172在锯齿卵圆形叶中表达量上调，参与植物逆境响应的保守的miR169、miR396在锯齿卵圆形叶中下调表达，推测差异表达miRNA引起了异形叶间形态的差异，同时使锯齿卵圆形叶对不利环境具有较强的耐受性。这与我们前期有关胡杨异形叶形态与生理特性的研究结果相一致。Abstract:ObjectiveHeterophylly is the phenomenon that plants form multiple types of mature leaves on the same plant to adapt to the environment. Populus euphratica is a typical woody heterophyllous plant, and previous research found that there were differences between heteromorphic leaves of P. euphratica in physiological characteristics and enironmental adaption. In this study, to reveal the molecular regulation of morphological and physiological characteristics in heteromorphic leaves of P. euphratica, we analyzed the differential expression of miRNAs and functions of target genes in heteromorphic leaves of P. euphratica.MethodIn this paper, using high-throughput sequencing, comparative study for miRNA expression patterns and functions of target genes was conducted in lanceolate leaves and dentate broad-ovate leaves.ResultTotal of 6 high-quality sRNA libraries were obtained, and the valid sequence of each library accounted for 56%−81% of the raw data. Total 517 known miRNAs and 127 predicted novel miRNAs were identified, the length of which was mainly distributed in 20−22 nt. Besides, 389 of the identified miRNAs were mapped to 54 known miRNA families, and there were 369 miRNAs detected in both two types of leaves. Compared with lanceolate leaves, 7 miRNAs were up-regulated and in dentate broad-ovate leaves, while 15 miRNAs were down-regulated. Based on the prediction of target genes and function annotation, differentially expressed miRNAs were involved in stress-resistant pathways in Populus euphratica, such as cellular response to salt stress, inositol phosphate metabolism, cutin, suberine and wax biosynthesis, base excision repair, and RNA degradation pathways. Moreover, expression levels of 5 differentially expressed miRNAs and their corresponding target genes were examined by quantitative real-time PCR, which could confirm the expression profile of the sRNA-sequencing and the negative regulation of miRNAs on their target genes.ConclusionOur study reveales that the expression patterns of miRNA between the heteromorphic leaves of P. euphratica are different. The miR167 and miR166 involved in growth and development of plant and miR172 associated with stress resistance of plant are up-regulated in dentate broad-ovate leaves. Besides, the miR169 and miR396 involved in stress resistance of plant are down-regulated in dentate broad-ovate leaves in comparison to lanceolate leaves. We speculate that the differential expression of miRNA may induce the morphological difference between heteromorphic leaves, and could increase the resistance of dentate broad-ovate leaves to adverse environments, this is consistent with our previous results of morphological and physiological characteristics in heteromorphic leaves of P. euphratica.
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图 1 胡杨两种典型异形叶
Figure 1. Two representative types of heteromorphic leaves in P. euphratica
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图 2 胡杨异形叶小RNA测序的有效序列长度分布统计
A. 总有效序列的长度分布；B.有效序列种类的长度分布。A, length distribution of total valid reads; B, length distribution of unique valid reads.
Figure 2. Length distribution of valid reads from sRNA sequencing for heteromorphic leaves in P. euphratica
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图 3 胡杨异形叶中miRNA统计分析
a. 胡杨异形叶miRNA碱基偏好性分析；b. 胡杨异形叶miRNA家族统计；c. 胡杨异形叶小RNA测序鉴定的已知miRNA及新发现miRNA的长度分布。a, miRNA nucleotide bias analysis of heteromorphic leaves in P. euphratica; b, miRNA family statistics of heteromorphic leaves in P. euphratica; c, length distribution of known miRNAs and novel miRNAs identified from sRNA sequencing for heteromorphic leaves in P. euphratica.
Figure 3. Statistical analysis of miRNA identified in heteromorphicleaves of P. euphratica
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图 4 胡杨异形叶miRNA检测的韦恩图及差异表达miRNA
A. 披针形叶片miRNA检测的韦恩图分析；B. 锯齿卵圆形叶片miRNA检测的韦恩图分析；C. 锯齿卵圆形与披针形叶片比较组中miRNA检测的韦恩图分析；D. 锯齿卵圆形与披针形叶片比较组中差异表达miRNA。A, Venn diagram of miRNA detected in lanceolate leaves; B, Venn diagram of miRNA detected in dentate broad-ovate leaves; C,Venn diagram of miRNA detected in dentate broad-ovate leaves vs lanceolate leaves group; D, differentially expressed miRNAs in dentate broad-ovate leaves vs lanceolate leaves group. Lan, lanceolate leaves; Db, dentate broad-ovate leaves.
Figure 4. Venn diagram of miRNA detected and differentially expressed miRNAs in heteromorphic leaves of P. euphratica
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图 5 胡杨异形叶中差异miRNA靶基因的GO注释
Figure 5. GO annotation of genes targeted by differentially expressed miRNA in heteromorphic leaves of P. euphratica
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图 6 差异miRNA靶基因的GO及KEGG通路富集性分析
A. 差异miRNA靶基因的GO富集性分析；B. 差异miRNA靶基因的KEGG通路富集性分析。A, analysis of GO enrichment of genes targeted by differentially expressed miRNAs; B, analysis of KEGG pathway enrichment of genes targeted by differentially expressed miRNAs.
Figure 6. Analysis of GO enrichment and KEGG pathway enrichment of genes targeted by differentially expressed miRNAs
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图 7 胡杨异形叶差异表达miRNA及靶基因的表达量分析
A. 差异miRNA的表达量分析；B. 差异miRNA的靶基因的表达量分析。图中误差棒表示平均值的标准偏差。A, analysis of expression level of the differentially expressed miRNAs; B, analysis of expression level of the target genes of differentially expressed miRNAs. Error bars show standard deviation of the average value.
Figure 7. Analysis of expression levels of the differentially expressed miRNAs and their target genes in heteromorphic leaves of P. euphratica
表 1 胡杨异形叶小RNA测序统计
Table 1 sRNA sequencing data from heteromorphic leaves in P. euphratica
文库 Library Lan_1 Lan_2 Lan_3 Db_1 Db_2 Db_3 总原始读段
Total raw reads10 994 672 10 095 826 9 811 531 9 849 631 10 445 363 10 587 269 唯一原始读段
Unique raw reads1 813 462 991 857 999 928 830 479 1 096 378 921 232 总3ADT及长度筛选
Total 3ADT & length filter4 491 129 3 357 910 1 750 389 1 604 935 4 096 241 1 930 624 总垃圾读段
Total junk reads28 511 11 988 15 331 15 505 12 559 16 490 总Rfam
Total Rfam168 570 95 671 79 962 93 630 53 066 112 629 总mRNA
Total mRNA300 609 128 948 131 286 148 439 143 075 196 224 总重复序列
Total repeats4 002 1 575 1 600 1 779 1 519 1 740 总有效读段
Total valid reads6 008 394 (54.65%) 6 502 632 (64.41%) 7 835 125 (79.86%) 7 988 626 (81.11%) 6 140 459 (58.79%) 8 333 317 (78.71%) 唯一有效读段
Unique valid reads1 130 544 (62.34%) 527 874 (53.22%) 745 979 (74.6%) 589 777 (71.02%) 664 491 (60.61%) 658 041 (71.43%) 注：Lan为披针形叶；Db为锯齿卵圆形叶。下同。Notes: Lan is lanceolate leaves; Db, dentate broad-ovate leaves. The same below. 
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表 2 胡杨异形叶miRNA鉴定统计
Table 2 Statistics of miRNA identification in heteromorphic leaves of P. euphratica
组别
GroupLan_1 Lan_2 Lan_3 Db_1 Db_2 Db_3 总数
Total组1
Group 13 4 3 3 3 4 4 组2
Group 2466 409 409 413 409 419 513 组3
Group 3114 79 97 98 90 97 127
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表 3 植物发育及环境响应相关的靶基因
Table 3 Target genes involved in plant development and environmental response
差异 miRNA
Differentially expressed miRNA差异表达
Differential expression靶基因登录号
Accession No. of target gene靶基因功能注释
Annotation of target geneptc-MIR169s-p3 下调
Down-regulatedXM_011048135.1, XM_011048134.1,
XM_011048132.1核转录因子Y
Nuclear transcription factor YXM_011024766.1, XM_011024764.1 GATA转录因子
GATA transcription factorptc-MIR396b-p3 下调
Down-regulatedXM_011046985.1 F-box蛋白
F-box proteinptc-miR167e 上调
Up-regulatedXM_011030586.1, XM_011030585.1,
XM_011030587.1, XM_011026286.1bHLH转录因子
bHLH transcription factorXM_011027709.1, XM_011027715.1,
XM_011027701.1, XM_011023286.1,
XM_011023287.1E3泛素蛋白连接酶E3
Ubiquitin-protein ligaseptc-MIR1450-p5_1ss12CG 下调
Down-regulatedXM_011028646.1, XM_011028647.1 阳离子质子反向运输载体
Cation/H（+）antiporterXM_011033752.1, XM_011047107.1,
XM_011047106.1ABC转运蛋白
ABC transporterXM_011036267.1 热休克蛋白
Heat shock proteinptc-MIR3627b-p3_2ss19TA20GA 下调
Down-regulatedXM_011044984.1 NAC转录因子
NAC transcription factor
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表 4 实时荧光定量PCR引物序列
Table 4 Primer sequence for quantitative real-time PCR
miRNA/mRNA 序列 Sequence (5′−3′) miRNA AGCAGGGTCCGAGGTATTC ptc-miR167e GTCGTATCCAGTGCAGGGTCCGAGGTATTCGCACTGGATACGACCAGATC ptc-miR167e CCGCGTGAAGCTGCCAGCAT lus-miR172j_L+1R-1 GTCGTATCCAGTGCAGGGTCCGAGGTATTCGCACTGGATACGACGGGAAT lus-miR172j_L+1R-1 CCGCGTGCAGCATCATCAAG ptc-miR169q_R+1_1ss14CT GTCGTATCCAGTGCAGGGTCCGAGGTATTCGCACTGGATACGACACAGGC ptc-miR169q_R+1_1ss14CT CCAGGCTAGCCAAGGACGATTT ptc-miR160b-3p GTCGTATCCAGTGCAGGGTCCGAGGTATTCGCACTGGATACGACTATGCA ptc-miR160b-3p CCAGCGTG GCGTATGAGGAGC ptc-MIR6474-p3_1ss21GT GTCGTATCCAGTGCAGGGTCCGAGGTATTCGCACTGGATACGACACTGTG ptc-MIR6474-p3_1ss21GT CCAGTCGACTATCTACGG XM_011030586.1 GATTTAGTGGAAGTTTTGCC XM_011030586.1 TAGCCTCTGTCATTTCATTG XM_011027061.1 ATGACGACGAGCACCCAA XM_011027061.1 CCATCTCAGACAATCCCTTT XM_011048135.1 CTGTTCAGGGAGCCATTT XM_011048135.1 CCATCATTCAACTCTTTCGT XM_011032166.1 CCAGGCATTGTTTATCGG XM_011032166.1 CCACAGTTGGGACATCAAGTATTA XM_011048960.1 AGTTAGTTTCAGAGGGTTGTG XM_011048960.1 CTTGTGGCAGCCATGTAG
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[1] Nakayama H, Nakayama N, Nakamasu A, et al. Toward elucidating the mechanisms that regulate heterophylly[J]. Plant Morphology, 2012, 24(1): 57−63. doi: 10.5685/plmorphol.24.57
[2] 叶元英, 柯卫东, 李峰, 等. 慈姑叶片结构的光学显微镜和扫描电镜观察[J]. 长江蔬菜, 2013(18):67−70. doi: 10.3865/j.issn.1001-3547.2013.18.022 Ye Y Y, Ke W D, Li F, et al. Observation of leaf structure of Chinese arrowhead (Sagittaria trifolia L.) by using optical microscope and scanning electron microscope[J]. Journal of Changjiang Vegetables, 2013(18): 67−70. doi: 10.3865/j.issn.1001-3547.2013.18.022
[3] Kordyum E, Klimenko E. Chloroplast ultrastructure and chlorophyll performance in the leaves of heterophyllous Nuphar lutea (L.) Smith. plants[J]. Aquatic Botany, 2013, 110: 84−91. doi: 10.1016/j.aquabot.2013.05.013
[4] Leigh A, Zwieniecki M A, Rockwell F E, et al. Structural and hydraulic correlates of heterophylly in Ginkgo biloba[J]. New Phytologist, 2011, 189(2): 459−470. doi: 10.1111/j.1469-8137.2010.03476.x
[5] Li G, Hu S, Yang J, et al. Water-wisteria as an ideal plant to study heterophylly in higher aquatic plants[J]. Plant Cell Reports, 2017, 36(8): 1225−1236. doi: 10.1007/s00299-017-2148-6
[6] 张金玲, 陈海鹏, 李玉灵, 等. 臭柏异形叶水分特性的比较[J]. 干旱区资源与环境, 2018(5):154−159. Zhang J L, Chen H P, Li Y L, et al. Comparison of water characteristics in the heterophylly of Sabina vulgaris[J]. Journal of Arid Land Resources and Environment, 2018(5): 154−159.
[7] Lee R C, Feinbaum R L, Ambros V. The C. elegans heterochronic gene lin-4 encodes small rnas with antisense complementarity to lin-14[J]. Cell, 1993, 75(5): 843−854. doi: 10.1016/0092-8674(93)90529-Y
[8] Sunkar R. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis[J]. Plant Cell, 2004, 16(8): 2001−2019. doi: 10.1105/tpc.104.022830
[9] Mi C E. Characterization of five microrna families in maize[J]. Journal of Experimental Botany, 2006, 57(11): 2601−2612. doi: 10.1093/jxb/erl013
[10] Arazi T, Talmor-Neiman M, Stav R, et al. Cloning and characterization of micro-RNAs from moss[J]. Plant Journal, 2005, 43(6): 837−848. doi: 10.1111/j.1365-313X.2005.02499.x
[11] Rajewsky N, Socci N D. Computational identification of microRNA targets[J]. Genome Biology, 2004, 5(2): 5−39. doi: 10.1186/gb-2004-5-2-p5
[12] 王杏茹, 李文静, 陈冰星, 等. 蕹菜耐受长时间高温后的miRNA分析[J]. 园艺学报, 2019, 46(3):486−498. Wang X R, Li W J, Chen B X, et al. Analysis of mirna in water spinach (Ipomoea aquatica) under long-time high temperature[J]. Acta Horticulturae Sinica, 2019, 46(3): 486−498.
[13] 彭廷, 文慧丽, 赵亚帆, 等. 盐、干旱胁迫下水稻相关miRNA的鉴定及表达分析[J]. 华北农学报, 2018, 33(2):20−27. Peng T, Wen H L, Zhao Y F, et al. Identification and expressions analysis of rice miRNA related to salt and drought stresses[J]. Acta Agriculture Boreali-Sinica, 2018, 33(2): 20−27.
[14] 司婧娜, 周韬, 徐放, 等. 胡杨无性系幼苗响应盐胁迫的miRNA表达差异研究[J]. 植物研究, 2015, 35(6):836−842. doi: 10.7525/j.issn.1673-5102.2015.06.008 Si J N, Zhou T, Xu F, et al. Salt-responsive microRNAs in Populus euphratica by deep sequencing[J]. Bulletin of Botanical Research, 2015, 35(6): 836−842. doi: 10.7525/j.issn.1673-5102.2015.06.008
[15] 郑彩霞, 邱箭, 姜春宁, 等. 胡杨多形叶气孔特征及光合特性的比较[J]. 林业科学, 2006, 42(8):19−24. doi: 10.3321/j.issn:1001-7488.2006.08.004 Zheng C X, Qiu J, Jiang C N, et al. Comparison of characteristics of stomas and photosynthesis of Populus euphratica polymorphic leaves[J]. Scientia Silvae Sinicae, 2006, 42(8): 19−24. doi: 10.3321/j.issn:1001-7488.2006.08.004
[16] 李萍萍, 曾明, 李文海, 等. 胡杨异形叶抗氧化能力的比较[J]. 北京林业大学学报, 2019, 41(8):76−83. Li P P, Zeng M, Li W H, et al. Comparative study on antioxidant capacity of heteromorphic leaves of Populus euphratica[J]. Journal of Beijing Forestry University, 2019, 41(8): 76−83.
[17] 韩航, 单凌飞, 王双蕾, 等. 胡杨异形叶光合作用特性研究[J]. 中央民族大学学报(自然科学版), 2019, 28(2):5−11. Han H, Shan L F, Wang S L, et al. Photosynthesis characteristics of heteromorphic leaves of Populus euphratica[J]. Journal of MUC (Natural Sciences Edition), 2019, 28(2): 5−11.
[18] Hao J, Yue N, Zheng C. Analysis of changes in anatomical characteristics and physiologic features of heteromorphic leaves in a desert tree, Populus euphratica[J]. Acta Physiologiae Plantarum, 2017, 39(8): 160−170. doi: 10.1007/s11738-017-2467-9
[19] 岳宁, 郑彩霞, 白雪, 等. 胡杨异形叶的蛋白质组学研究[J]. 中国生物工程杂志, 2009, 29(9):40−44. Yue N, Zheng C X, Bai X, et al. Proteomics analysis of heteromorphic leaves of Populus euphratica Oliv.[J]. China Biotechnology, 2009, 29(9): 40−44.
[20] Bo X, Wang S. TargetFinder: a software for antisense oligonucleotide target site selection based on MAST and secondary structures of target mRNA[J]. Bioinformatics, 2005, 21(8): 1401−1402. doi: 10.1093/bioinformatics/bti211
[21] Wang H L, Lan L, Sha T, et al. Evaluation of appropriate reference genes for reverse transcription-quantitative PCR studies in different tissues of a desert poplar via comparision of different algorithms[J]. International Journal of Molecular Sciences, 2015, 16(9): 20468−20491. doi: 10.3390/ijms160920468
[22] Livak K, Schmittgen T. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ CT method[J]. Methods, 2000, 25(4): 402−408.
[23] Nakayama H, Nakayama N, Seiki S, et al. Regulation of the KNOX-GA gene module induces heterophyllic alteration in North American Lake Cress[J]. The Plant Cell Online, 2015, 26(12): 4733−4748.
[24] Nakayama H, Sinha N R, Kimura S. How do plants and phytohormones accomplish heterophylly, leaf phenotypic plasticity, in response to environmental cues[J]. Frontiers in Plant Science, 2017, 8: 10−17.
[25] Zhang B, Pan X, Cobb G P, et al. Plant microRNA: a small regulatory molecule with big impact[J]. Developmental Biology, 2006, 289(1): 3−16.
[26] Zeng M, He S, Hao L, et al. Conjoint analysis of genome-wide lncRNA and mRNA expression of heteromorphic leaves in response to environmental heterogeneity in Populus euphratica[J]. International Journal of Molecular Sciences, 2019, 20: 5148−5871. doi: 10.3390/ijms20205148
[27] 白雪, 张淑静, 郑彩霞, 等. 胡杨多态叶光合和水分生理的比较[J]. 北京林业大学学报, 2011, 33(6):47−52. Bai X, Zhang S J, Zheng C X, et al. Comparative study on photosynthesis and water physiology of polymorphic leaves of Populus euphratica[J]. Journal of Beijing Forestry University, 2011, 33(6): 47−52.
[28] 王海珍, 韩路, 徐雅丽, 等. 胡杨异形叶叶绿素荧光特性对高温的响应[J]. 生态学报, 2011, 31(9):2444−2453. Wang H Z, Han L, Xu Y L, et al. Response of chlorophyll fluorescence characteristics of Populus euphratica heteromorphic leaves to high temperature[J]. Acta Ecologica Sinica, 2011, 31(9): 2444−2453.
[29] Abel K, Anderson R A, Shears S B. Phosphatidylinositol and inositol phosphate metabolism[J]. Journal of Cell Science, 2001, 114: 2207−2208.
[30] Samuels L, Kunst L, Jetter R. Sealing plant surfaces: cuticular wax formation by epidermal cells[J]. Annual Review of Plant Biology, 2008, 59(1): 683−707. doi: 10.1146/annurev.arplant.59.103006.093219
[31] Liu Y, Li X, Chen G, et al. Epidermal micromorphology and mesophyll structure of Populus euphratica heteromorphic leaves at different development stages[J/OL]. PLoS ONE, 2015, 10: e137701 (2015−10−09) [2018−05−21]. https://doi.org/10.1371/jounal.pone.0137701.
[32] Mannuss A, Trapp O, Puchta H. Gene regulation in response to DNA damage[J]. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 2012, 1819(2): 154−165. doi: 10.1016/j.bbagrm.2011.08.003
[33] Chen J, Zhang J, Hu J, et al. Integrated regulatory network reveals the early salt tolerance mechanism of Populus euphratica[J]. Scientific Reports, 2017, 7(1): 6769−6781. doi: 10.1038/s41598-017-05240-0
[34] 曾幼玲, 杨瑞瑞. 植物miRNA的生物学特性及在环境胁迫中的作用[J]. 中国农业科学, 2016, 49(19):3671−3682. doi: 10.3864/j.issn.0578-1752.2016.19.001 Zeng Y L, Yang R R. Biological characteristics of plant microRNAs and actions in environmental stresses[J]. Scientia Agricultura Sinica, 2016, 49(19): 3671−3682. doi: 10.3864/j.issn.0578-1752.2016.19.001
[35] 韦懿, 陈志辉, 陈国兴, 等. 超量表达水稻miRNA 167A调控株型的研究[J]. 分子植物育种, 2011, 9(4):390−396. doi: 10.3969/mpb.009.000390 Wei Y, Chen Z H, Chen G X, et al. Study of overexpressing miRNA167a to regulate the architecture in Oryza sativa[J]. Molecular Plant Breeding, 2011, 9(4): 390−396. doi: 10.3969/mpb.009.000390
[36] Merelo P, Ram H, Caggiano M P, et al. Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity[J]. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(42): 11973−11978. doi: 10.1073/pnas.1516110113
[37] 张文政, 韩颖颖, 严钦骅, 等. 拟南芥miR172a-1/b-2/c对多种胁迫响应的研究[J]. 复旦学报( 自然科学版), 2011, 50(3):328−333. Zhang W Z, Han Y Y, Yan Q H, et al. Research of arabidopsis miR172a-1/b-2/c in response to multiple stresses[J]. Journal of Fudan University (Natural Science), 2011, 50(3): 328−333.
[38] Li W, Wang T, Zhang Y, et al. Overexpression of soybean miR172c confers water deficit and salt tolerance but ABA sensitivity in transgenic Arabidopsis thaliana[J]. Journal of Experimental Botany, 2015, 67(1): 175−194.
[39] 栾明达. 玉米miR169及其靶基因NF-YA转录因子功能的初步研究[D]. 绵阳: 西南科技大学, 2014. Luan M D. Research of zma-miR169s and their targeted transcription factor ZmNF-YAs in maize [D]. Mianyang: Southwest University of Science and Technology, 2014.
[40] 叶超楠, 沈栎阳, 方春, 等. 热胁迫下水稻miR396家族及靶基因OsGRFs的表达研究[J]. 农业生物技术学报, 2018, 26(3):393−400. Ye C N, Shen L Y, Fang C, et al. Expression analysis of rice (Oryza sativa) miR396 family and target gene OsGRFs under heat stress[J]. Journal of Agricultural Biotechnology, 2018, 26(3): 393−400.
[41] Lian C, Li Q, Yao K, et al. Populus trichocarpa PtNF-YA9, a multifunctional transcription factor, regulates seed germination, abiotic stress, plant growth and development in Arabidopsis [J/OL]. Frontiers in Plant Science, 2018, 9: 1403 (2018−07−09)[2018−12−20]. https://doi.org/10.3389/fpls.2018.01403.
[42] Yan D, Sha T, Xia X, et al. Identification of PeNF-YB1 expressed in leaves of Populus euphratica responsive to drought[J]. Chinese Agricultural Science Bulletin, 2012, 28(19): 6−11.
[43] Yi A, Yangyan Z, Xiao H, et al. The GATA transcription factor GNC plays an important role in photosynthesis and growth in poplar[J]. Journal of Experimental Botany, 2019, 71(6): 1969−1984.
[44] 任逸秋, 贾会霞, 郭英华, 等. 胡杨F-Box基因克隆和功能分析[J]. 分子植物育种, 2017, 15(5):1655−1662. Ren Y Q, Jia H X, Guo Y H, et al. Identification and functional analysis of F-Box gene from Populus euphratica[J]. Molecular Plant Breeding, 2017, 15(5): 1655−1662.
[45] Zhang L Y, Bai M Y, Wu J, et al. Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis[J]. Plant Cell, 2009, 21(12): 3767−3780. doi: 10.1105/tpc.109.070441
[46] Dong Y, Wang C, Han X, et al. A novel bHLH transcription factor PebHLH35 from Populus euphratica confers drought tolerance through regulating stomatal development, photosynthesis and growth in arabidopsis[J]. Biochemical & Biophysical Research Communications, 2014, 450(1): 453−458.
[47] 钱泽勇, 张会龙, 荆晓姝, 等. 胡杨Ring Finger E3连接酶PeRH2提高烟草耐旱机制研究[J]. 基因组学与应用生物学, 2015, 34(3):454−463. Qian Z Y, Zhang H L, Jing X S, et al. Overexpression of RING finger E3-ligase gene PeRH2 from Populus euphratica in tobacco enhances drought tolerance in transgenic plants[J]. Genomics and Applied Biology, 2015, 34(3): 454−463.
[48] Fang H, Wang H L, Li H G, et al. PeCHYR1, a ubiquitin E3 ligase from Populus euphratica, enhances drought tolerance via ABA-induced stomatal closure by ROS production in Populus[J]. Plant Biotechnology Journal, 2018, 16(8): 1514−1528. doi: 10.1111/pbi.12893
[49] Silva P, Faanha A R, Rui M T, et al. Role of tonoplast proton pumps and Na+/H+ antiport system in salt tolerance of Populus euphratica Oliv.[J]. Journal of Plant Growth Regulation, 2010, 29(1): 23−34. doi: 10.1007/s00344-009-9110-y
[50] Wang L, Feng X, Zhao H, et al. Functional analysis of the Na+, K+/H+ antiporter PeNHX3 from the tree halophyte Populus euphratica in yeast by model-guided mutagenesis[J]. Plos One, 2014, 9(8): e104147(2015−02−03)[2018−04−22]. https://doi.org/10.1371/journal.pone.0117869.
[51] Wu Y, Meng K, Liang X. Distinct patterns of natural selection in Na+/H+ antiporter genes in Populus euphratica and Populus pruinosa[J]. Ecology & Evolution, 2017, 7(1): 82−91.
[52] Pighin J A, Huanquan Z, Balakshin L J, et al. Plant cuticular lipid export requires an ABC transporter[J]. Science, 2004, 306: 702−704. doi: 10.1126/science.1102331
[53] Ningmei C, Buerbatu S, Shuai T, et al. Overexpression of the ABC transporter gene TsABCG11 increases cuticle lipids and abiotic stress tolerance in arabidopsis[J]. Plant Biotechnology Reports, 2018, 12(5): 303−313. doi: 10.1007/s11816-018-0495-6
[54] Yan D H, Fenning T, Tang S, et al. Genome-wide transcriptional response of Populus euphratica to long-term drought stress[J]. Plant Science, 2012, 195: 24−35. doi: 10.1016/j.plantsci.2012.06.005
[55] Wang J Y, Wang J, He Y. A Populus euphratica NAC protein regulating Na+/K+ homeostasis improves salt tolerance in Arabidopsis thaliana[J]. Gene, 2013, 521(2): 265−273. doi: 10.1016/j.gene.2013.03.068
[56] Lu X, Zhang X, Duan H, et al. Three stress-responsive NAC transcription factors from Populus euphratica differentially regulate salt and drought tolerance in transgenic plants[J]. Physiologia Plantarum, 2018, 162(1): 73−97. doi: 10.1111/ppl.12613
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