Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (10): 1995-2009.doi: 10.3864/j.issn.0578-1752.2024.10.011

• HORTICULTURE • Previous Articles     Next Articles

Transcriptome Analysis for Screening Key Genes Related to Regulating Branching Ability in Apple

ZHANG HaiQing(), ZHANG HengTao, GAO QiMing, YAO JiaLong, WANG YaRong, LIU ZhenZhen, MENG XiangPeng, ZHOU Zhe(), YAN ZhenLi()   

  1. Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou 450009
  • Received:2023-11-01 Accepted:2024-03-29 Online:2024-05-16 Published:2024-05-23
  • Contact: ZHOU Zhe, YAN ZhenLi

Abstract:

【Background】 The number of branches on an apple tree plays a pivotal role in its environmental adaptability, growth, survival, and resource competition. In production practice, the apple cultivars with more branches can better meet the needs of pruning and shaping, not only do they facilitate timely adjustments to the tree's structure based on local conditions, but also they ensure a uniform distribution of fruit-bearing branches, thereby guaranteeing both fruit quantity and quality. 【Objective】 In this study, by using the top buds and lateral buds of more-branched cultivar Huaxing and fewer-branched cultivar Huashuo at the same developmental stage, the transcriptome sequencing was carried out to identify key genes regulating the ability of branching, as well as to elucidate the potential mechanism underlying branching phenotype, and finally to provide the theoretical basis for improving the branching ability and yield of apple. 【Method】 The lateral and terminal buds of Huashuo and Huaxing were sampled for RNA-seq. By differential expressed gene (DEG) and analysis and weighted gene co-expression network (WGCNA) analysis, the core candidate genes that were responsible for branch number difference were identified and further demonstrated their function by Arabidopsis transformation.【Result】 A total of 2 920 DEGs were identified from the comparison between the terminal buds, while 5 127 DEGs were screened out from the comparison between the lateral buds. DEGs were mainly enriched in phytohormone signaling pathway. Notably, the auxin signaling pathway, and strigolactone signaling pathway seemed to have the closest connection with the branching ability of apple with the related genes encoding MdIAA3, MAX2, TCP, and JAZ, which showed significant differences between lateral buds. Furthermore, DEGs annotated to cell cycle and cell wall modification families, such as CYC (Cyclins), CDK (Cyclin-dependent kinase), and EXPA (Expansin), also demonstrated a positive correlation with apple branching ability. In addition, those candidate genes obtained from WGCNA analysis also showed high possibility of getting involved in branch number regulation. Heterologous transformation of Arabidopsis with MdIAA3 could significantly enhance the overall growth, increased pod number and branching number of Arabidopsis. 【Conclusion】 Through comprehensive research, 13 candidate regulatory genes were identified that potentially played a crucial role in transcriptional regulation for branch number. MdIAA3 was ectopically expressed in Arabidopsis, which significantly promoted plant growth and branching ability. It was plausible that these genes regulated branching through processes, such as cell differentiation and development, cell wall modification, auxin, and strigolactone signaling pathway.

Key words: apple, branching ability, transcriptome analysis, KEGG, plant hormone, MdIAA3

Fig. 1

Less-branched Huashuo (left) and more-branched Huaxing (right)"

Table 1

Sequencing data statistics"

样本
Sample
原始序列数据
Raw reads
过滤后数据
Clean reads
比对到基因组
Total map
碱基质量值
Q20 (%)
碱基质量值
Q30 (%)
GC占比
GC (%)
HSD1 46230010 45481100 40805210(89.72%) 96.07 89.95 45.42
HSD2 47417824 46744010 42366223(90.63%) 96.57 90.97 46.07
HSD3 50614470 49588586 44958745(90.66%) 96.64 91.07 46.12
HSC1 41885282 40719076 36228477(88.97%) 96.07 90.07 46.07
HSC2 45343404 44619430 40058699(89.78%) 96.72 91.30 45.85
HSC3 41242840 40301052 36008246(89.35%) 96.45 90.78 45.93
HXD1 46239534 45644466 41374789(90.65%) 95.94 89.81 46.15
HXD2 46475308 45429544 41069245(90.40%) 96.46 90.81 46.43
HXD3 45253168 44460432 40627835(91.38%) 96.88 91.66 46.50
HXC1 42828110 42435144 38346254(90.36%) 96.29 90.44 45.92
HXC2 46425522 45877734 41220790(89.85%) 95.96 89.79 45.53
HXC3 46221574 45743482 41406160(90.52%) 96.67 91.20 45.61

Fig. 2

Sample principal component analysis (A) and correlation analysis (B)"

Fig. 3

Analysis of differentially expressed genes between terminal and lateral buds of Huashuo and Huaxing A: DEGs Venn diagram of terminal and lateral buds of Huashuo and Huaxing cultivars; B: DEGs statistics of terminal bud and lateral bud between cultivars of Huashuo and Huaxing; C: DEGs volcano maps of terminal bud between cultivars of Huashuo and Huaxing; D: DEGs volcano maps of lateral bud between cultivars of Huashuo and Huaxing"

Fig. 4

KEGG enrichment analysis of DEGs The results show only the top 20 metabolic pathways with the most significant enrichment. A: Terminal bud KEGG enrichment analysis; B: Lateral bud KEGG enrichment analysis"

Fig. 5

Analysis of differential gene expression related to plant hormone signal transduction The heatmap depicts the expression of related genes among HSD, HXD, HSC, and HXC based on Log10 (FPKM). A: Auxin related genes; B: Cytokinin related genes; C: Strigolactone related genes; D: Abscisic acid related genes; E: Jasmonic acid related genes; F: Differences in endogenous hormone levels"

Fig. 6

Gene expression analysis of cell wall modification A: Cell cycle related genes; B: Cell wall modification related genes"

Fig. 7

Analysis of WGCNA between terminal and lateral buds of Huashuo and Huaxing A:Network analysis dendrogram showing modules identified by weighted gene co-expression network analysis (WGCNA); B: Correlation analysis between module and sample phenotype; C: The coexpression network of core genes in the terminal and lateral buds modules of Huashuo and Huaxing. EXPA: Expansin A; CYC: Cyclins; JAZ: Jjasmonate ZIM-domain; CAD: Cinnamyl alcohol dehydrogenase; SAUR: Small auxin up RNA"

Fig. 8

Heterologous transformation of Arabidopsis by MdIAA3 A: Relative expression of WT and different transgenic lines; B: Comparison of WT and transgenic lines MdIAA3OX-18 and MdIAA3OX-6 strains with higher relative expression"

[1]
MASHIGUCHI K, TANAKA K, SAKAI T, SUGAWARA S, KAWAIDE H, NATSUME M, HANADA A, YAENO T, SHIRASU K, YAO H, MCSTEEN P, ZHAO Y D, HAYASHI K I, KAMIYA Y, KASAHARA H. The main auxin biosynthesis pathway in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(45): 18512-18517.
[2]
SHIMIZU-SATO S, MORI H. Control of outgrowth and dormancy in axillary buds. Plant Physiology, 2001, 127(4): 1405-1413.
[3]
HILL J L, HOLLENDER C A. Branching out: new insights into the genetic regulation of shoot architecture in trees. Current Opinion in Plant Biology, 2019, 47: 73-80.

doi: S1369-5266(18)30030-X pmid: 30339931
[4]
FERGUSON B J, BEVERIDGE C A. Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiology, 2009, 149(4): 1929-1944.

doi: 10.1104/pp.109.135475 pmid: 19218361
[5]
SU Y H, LIU Y B, ZHANG X S. Auxin-cytokinin interaction regulates meristem development. Molecular Plant, 2011, 4(4): 616-625.
[6]
SWARUP R, BHOSALE R. Developmental roles of AUX1/LAX auxin influx carriers in plants. Frontiers in Plant Science, 2019, 10: 1306.

doi: 10.3389/fpls.2019.01306 pmid: 31719828
[7]
ASGHAR S, XIONG Y, CHE M, FAN X Q, LI H, WANG Y, XU X F, LI W, HAN Z H. Transcriptome analysis reveals the effects of strigolactone on shoot regeneration of apple. Plant Cell Reports, 2022, 41(7): 1613-1626.

doi: 10.1007/s00299-022-02882-x pmid: 35680714
[8]
KHUVUNG K, SILVA GUTIERREZ F A O, REINHARDT D. How strigolactone shapes shoot architecture. Frontiers in Plant Science, 2022, 13: 889045.
[9]
UMEHARA M, HANADA A, YOSHIDA S, AKIYAMA K, ARITE T, TAKEDA-KAMIYA N, MAGOME H, KAMIYA Y, SHIRASU K, YONEYAMA K, KYOZUKA J, YAMAGUCHI S. Inhibition of shoot branching by new terpenoid plant hormones. Nature, 2008, 455: 195-200.
[10]
LJUNG K, BHALERAO R P, SANDBERG G. Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. The Plant Journal, 2001, 28(4): 465-474.
[11]
MÜLLER D, LEYSER O. Auxin, cytokinin and the control of shoot branching. Annals of Botany, 2011, 107(7): 1203-1212.

doi: 10.1093/aob/mcr069 pmid: 21504914
[12]
DIERCK R, DE KEYSER E, DE RIEK J, DHOOGHE E, VAN HUYLENBROECK J, PRINSEN E, VAN DER STRAETEN D. Change in auxin and cytokinin levels coincides with altered expression of branching genes during axillary bud outgrowth in Chrysanthemum. PLoS ONE, 2016, 11(8): e0161732.
[13]
SHINOHARA N, TAYLOR C, LEYSER O. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biology, 2013, 11(1): e1001474.
[14]
沈月, 陶宝杰, 华夏, 吕冰, 刘立军, 陈云. 独脚金内酯与激素互作调控根系生长的研究进展. 生物技术通报, 2022, 38(8): 24-31.

doi: 10.13560/j.cnki.biotech.bull.1985.2022-0102
SHEN Y, TAO B J, HUA X, B, LIU L J, CHEN Y. Research progress in the interactions of strigolactone with hormones on regulating root growth. Biotechnology Bulletin, 2022, 38(8): 24-31. (in Chinese)

doi: 10.13560/j.cnki.biotech.bull.1985.2022-0102
[15]
刘丛丛. 生长素及独脚金内酯通过细胞分裂素调控番茄侧枝生长发育的机制研究[D]. 杭州: 浙江大学, 2017.
LIU C C. The mechanisms of auxin and strigolactone control lateral branching outgrowth through cytokinin in tomato plants[D]. Hangzhou: Zhejiang University, 2017. (in Chinese)
[16]
JIANG L, LIU X, XIONG G S, LIU H H, CHEN F L, WANG L, MENG X B, LIU G F, YU H, YUAN Y D, YI W, ZHAO L H, MA H L, HE Y Z, WU Z S, MELCHER K, QIAN Q, XU H E, WANG Y H, LI J Y. DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature, 2013, 504: 401-405.
[17]
LIU X, HU Q L, YAN J J, SUN K, LIANG Y, JIA M R, MENG X B, FANG S, WANG Y Q, JING Y H, LIU G F, WU D X, CHU C C, SMITH S M, CHU J F, WANG Y H, LI J Y, WANG B. ζ-carotene isomerase suppresses tillering in rice through the coordinated biosynthesis of strigolactone and abscisic acid. Molecular Plant, 2020, 13(12): 1784-1801.

doi: 10.1016/j.molp.2020.10.001 pmid: 33038484
[18]
LIU R X, FINLAYSON S A. Sorghum tiller bud growth is repressed by contact with the overlying leaf. Plant, Cell & Environment, 2019, 42(7): 2120-2132.
[19]
DONG Z B, XIAO Y G, GOVINDARAJULU R, FEIL R, SIDDOWAY M L, NIELSEN T, LUNN J E, HAWKINS J, WHIPPLE C, CHUCK G. The regulatory landscape of a core maize domestication module controlling bud dormancy and growth repression. Nature Communications, 2019, 10: 3810.

doi: 10.1038/s41467-019-11774-w pmid: 31444327
[20]
JIANG Z H, ZHOU X, LI R, MICHAL J J, ZHANG S W, DODSON M V, ZHANG Z W, HARLAND R M. Whole transcriptome analysis with sequencing: methods, challenges and potential solutions. Cellular and Molecular Life Sciences, 2015, 72(18): 3425-3439.

doi: 10.1007/s00018-015-1934-y pmid: 26018601
[21]
LANGFELDER P, HORVATH S. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 2008, 9: 559.

doi: 10.1186/1471-2105-9-559 pmid: 19114008
[22]
TANG Y W, LI J H, SONG Q Q, CHENG Q, TAN Q L, ZHOU Q G, NONG Z M, LV P. Transcriptome and WGCNA reveal hub genes in sugarcane tiller seedlings in response to drought stress. Scientific Reports, 2023, 13: 12823.

doi: 10.1038/s41598-023-40006-x pmid: 37550374
[23]
谭西北, 李鹏, 孙磊, 樊秀彩, 刘崇怀, 姜建福, 张颖. 基于WGCNA的刺葡萄抗白腐病关键基因的发掘. 果树学报, 2023, 40(4): 653-668.
TAN X B, LI P, SUN L, FAN X C, LIU C H, JIANG J F, ZHANG Y. Discovery of key genes for White Rot resistance in Vitis davidii based on WGCNA. Journal of Fruit Science, 2023, 40(4): 653-668. (in Chinese)
[24]
CHEN C J, CHEN H, ZHANG Y, THOMAS H R, FRANK M H, HE Y H, XIA R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 2020, 13(8): 1194-1202.

doi: S1674-2052(20)30187-8 pmid: 32585190
[25]
ZHANG Y, DU D D, WEI H L, XIE S N, TIAN X C, YANG J, XIAO S Q, TANG Z H, LI D W, LIU Y. Transcriptomic and hormone analyses provide insight into the regulation of axillary bud outgrowth of Eucommia ulmoides oliver. Current Issues in Molecular Biology, 2023, 45(9): 7304-7318.
[26]
李司敏. 水稻Aux/IAA基因家族进化分析及OsIAA23基因功能的鉴定[D]. 南京: 南京大学, 2019.
LI S M. Evolutionary analysis of aux/IAA gene family in rice and functional identification of OsIAA23[D]. Nanjing: Nanjing University, 2019. (in Chinese)
[27]
SU B H, WU H T, GUO Y, GAO H W, WEI Z Y, ZHAO Y Y, QIU L J. GmIAA27 encodes an AUX/IAA protein involved in dwarfing and multi-branching in soybean. International Journal of Molecular Sciences, 2022, 23(15): 8643.
[28]
LIU S D, HU Q N, LUO S, LI Q Q, YANG X Y, WANG X L, WANG S C. Expression of wild-type PtrIAA14.1, a poplar Aux/IAA gene causes morphological changes in Arabidopsis. Frontiers in Plant Science, 2015, 6: 388.
[29]
HOU Y M, LI H X, ZHAI L L, XIE X, LI X Y, BIAN S M. Identification and functional characterization of the Aux/IAA gene VcIAA27 in blueberry. Plant Signaling & Behavior, 2020, 15(1): 1700327.
[30]
JEZ J M. Connecting primary and specialized metabolism: Amino acid conjugation of phytohormones by GRETCHEN HAGEN 3 (GH3) acyl acid amido synthetases. Current Opinion in Plant Biology, 2022, 66: 102194.
[31]
DOMAGALSKA M A, LEYSER O. Signal integration in the control of shoot branching. Nature Reviews Molecular Cell Biology, 2011, 12: 211-221.

doi: 10.1038/nrm3088 pmid: 21427763
[32]
陈奋奇, 张金青, 马晖玲. 激素调控植物分枝/分蘖的研究进展. 草业学报, 2024, 33(2): 212-225.

doi: 10.11686/cyxb2023118
CHEN F Q, ZHANG J Q, MA H L. Progress of research on hormone regulation of branching or tillering in plants. Acta Prataculturae Sinica, 2024, 33(2): 212-225. (in Chinese)
[33]
檀鸣. 苹果MdWUS2介导细胞分裂素抑制MdTCP12调控腋芽萌发的分子机制研究[D]. 杨凌: 西北农林科技大学, 2019.
TAN M. Molecular mechanism of MdWUS2 mediating cytokinin inhibition of MdTCP12 in regulating axillary bud outgrowth in Malus [D]. Yangling: Northwest A & F University, 2019. (in Chinese)
[34]
刘杨. 苹果细胞分裂素氧化酶/脱氢酶基因MdCKX5.2的克隆和功能鉴定[D]. 泰安: 山东农业大学, 2022.
LIU Y. Molecular cloning and functional characterization of cytokinin oxidase/dehydrogenases gene MdCKX5.2 in apple[D]. Taian: Shandong Agricultural University, 2022. (in Chinese)
[35]
BÜRGER M, CHORY J. The many models of strigolactone signaling. Trends in Plant Science, 2020, 25(4): 395-405.

doi: S1360-1385(19)30334-6 pmid: 31948791
[36]
程方. 苹果独脚金内酯合成基因MdMAX1调控腋芽萌发的功能研究[D]. 杨凌: 西北农林科技大学, 2020.
CHENG F. Functional analysis of strigolactone biosynthesis gene MdMAX1 in the regulation of axillary bud outgrowth in apple[D]. Yangling: Northwest A & F University, 2020. (in Chinese)
[37]
李国防. 苹果MAX2基因介导独脚金内酯信号调控腋芽萌发的功能研究[D]. 杨凌: 西北农林科技大学, 2018.
LI G F. Functional study of MAX2 gene on the regulation of axillary bud outgrowth by mediating strigolactone signaling in Malus[D]. Yangling: Northwest A & F University, 2018. (in Chinese)
[38]
WANG L, WANG B, YU H, GUO H Y, LIN T, KOU L Q, WANG A Q, SHAO N, MA H Y, XIONG G S, LI X Q, YANG J, CHU J F, LI J Y. Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature, 2020, 583: 277-281.
[39]
LUO L, TAKAHASHI M, KAMEOKA H, QIN R Y, SHIGA T, KANNO Y, SEO M, ITO M, XU G H, KYOZUKA J. Developmental analysis of the early steps in strigolactone-mediated axillary bud dormancy in rice. The Plant Journal, 2019, 97(6): 1006-1021.

doi: 10.1111/tpj.14266 pmid: 30740793
[40]
杨永岗, 张化生, 李晓芳, 苏永全. 不同分枝西瓜品种生长过程中内源激素含量的变化. 中国蔬菜, 2020(10): 48-54.
YANG Y G, ZHANG H S, LI X F, SU Y Q. Changes of endogenous hormone content in watermelon varieties with different branching forms during their growth process. China Vegetables, 2020(10): 48-54. (in Chinese)
[41]
王肖凤. 茉莉酸类物质促进再生稻再生芽解除休眠和水分管理影响再生稻稻米品质的研究[D]. 武汉: 华中农业大学, 2021.
WANG X F. JAs promote the breaking dormancy of ratoon buds in ratoon rice and effects of water management on grain quality[D]. Wuhan: Huazhong Agricultural University, 2021. (in Chinese)
[42]
DONG N Q, LIN H X. Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. Journal of Integrative Plant Biology, 2021, 63(1): 180-209.
[43]
闵卓. 独脚金内酯诱导VviBRCs基因参与葡萄夏芽萌发的调控机理解析[D]. 杨凌: 西北农林科技大学, 2019.
MIN Z. Study on the mechanism of exogenous strigolactones regulating grape prompt bud outgrowth by VviBrc genes[D]. Yangling: Northwest A & F University, 2019. (in Chinese)
[44]
OHYAMA A, TOMINAGA R, TORIBA T, TANAKA W. D-type cyclin OsCYCD3;1 is involved in the maintenance of meristem activity to regulate branch formation in rice. Journal of Plant Physiology, 2022, 270: 153634.
[45]
张珂. 甘蔗腋芽萌发相关植物激素代谢分析及促萌发诱导剂的筛选[D]. 福州: 福建农林大学, 2020.
ZHANG K. Metabolic analysis of plant hormones related to germination of sugarcane axillary buds and screening of germination inducer[D]. Fuzhou: Fujian Agriculture and Forestry University, 2020. (in Chinese)
[46]
WEISS D, ORI N. Mechanisms of cross talk between gibberellin and other hormones. Plant Physiology, 2007, 144(3): 1240-1246.

pmid: 17616507
[47]
XU J X, ZHA M R, LI Y, DING Y F, CHEN L, DING C Q, WANG S H. The interaction between nitrogen availability and auxin, cytokinin, and strigolactone in the control of shoot branching in rice (Oryza sativa L.). Plant Cell Reports, 2015, 34(9): 1647-1662.
[48]
HAYASHI K I, ARAI K, AOI Y, TANAKA Y, HIRA H, GUO R P, HU Y, GE C N, ZHAO Y D, KASAHARA H, FUKUI K. The main oxidative inactivation pathway of the plant hormone auxin. Nature Communications, 2021, 12: 6752.
[49]
陈潇. 番茄吲哚-3-乙酸氨基合成酶基因SlGH3.4在丛枝菌根共生中的功能和调控机制研究[D]. 南京: 南京农业大学, 2017.
CHEN X. The roles and regulatory mechanisms of A putative tomato indole-3-acetic acid amido synthetase gene, Slgh3.4, in the establishment of arbuscular mycorrhizal symbiosis[D]. Nanjing: Nanjing Agricultural University, 2017. (in Chinese)
[50]
李孟湛. SAUR15调控植物侧根及不定根发育的功能及分子机理研究[D]. 兰州: 兰州大学, 2022.
LI M Z. Functions and molecular mechanisms of SAUR15 in regulating development of plant lateral and adventitious roots[D]. Lanzhou: Lanzhou University, 2022. (in Chinese)
[51]
张焕凯. 生长素响应因子ARF3通过组蛋白乙酰化修饰调控拟南芥顶端分生组织干细胞的维持[D]. 泰安: 山东农业大学, 2020.
ZHANG H K. Auxin response factor 3 specifies stem cells in apical meristem via mediating an auxin-responsive histone acetylation in Arabidopsis [D]. Taian: Shandong Agricultural University, 2020. (in Chinese)
[52]
JUNG H, LEE D K, DO CHOI Y, KIM J K. OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Science, 2015, 236: 304-312.

doi: 10.1016/j.plantsci.2015.04.018 pmid: 26025543
[53]
WANG L, WANG B, JIANG L, LIU X, LI X L, LU Z F, MENG X B, WANG Y H, SMITH S M, LI J Y. Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. The Plant Cell, 2015, 27(11): 3128-3142.
[54]
STIRNBERG P, VAN DE SANDE K, OTTOLINE LEYSER H M. MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development, 2002, 129(5): 1131-1141.
[55]
WANG X X, WEI J, WU J H, SHI B J, WANG P H, ALABD A, WANG D N, GAO Y H, NI J B, BAI S L, TENG Y W. Transcription factors BZR2/MYC2 modulate brassinosteroid and jasmonic acid crosstalk during pear dormancy. Plant Physiology, 2024, 194(3): 1794-1814.
[56]
ONGARO V, LEYSER O. Hormonal control of shoot branching. Journal of Experimental Botany, 2008, 59(1): 67-74.

doi: 10.1093/jxb/erm134 pmid: 17728300
[57]
HORVATH D P, CHAO W S, ANDERSON J V. Molecular analysis of signals controlling dormancy and growth in underground adventitious buds of leafy spurge. Plant Physiology, 2002, 128(4): 1439-1446.

doi: 10.1104/pp.010885 pmid: 11950992
[58]
FREEMAN D, RIOU-KHAMLICHI C, OAKENFULL E A, MURRAY J A H. Isolation, characterization and expression of cyclin and cyclin-dependent kinase genes in Jerusalem artichoke (Helianthus tuberosus L.). Journal of Experimental Botany, 2003, 54(381): 303-308.
[59]
GOH H H, SLOAN J, MALINOWSKI R, FLEMING A. Variable expansin expression in Arabidopsis leads to different growth responses. Journal of Plant Physiology, 2014, 171(3/4): 329-339.
[60]
ROMAN H, GIRAULT T, LE GOURRIEREC J, LEDUC N. In silico analysis of 3 expansin gene promoters reveals 2 hubs controlling light and cytokinins response during bud outgrowth. Plant Signaling & Behavior, 2017, 12(2): e1284725.
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