Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (6): 1195-1209.doi: 10.3864/j.issn.0578-1752.2025.06.011

• HORTICULTURE • Previous Articles     Next Articles

Analysis of Conserved Genes in Adventitious Root Formation Based on Cross Species Transcriptomes

XIE LuLu(), LI Fu, ZHANG SiYuan, GAO JianChang()   

  1. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences/State Key Laboratory of Vegetable Biobreeding, Beijing 100081
  • Received:2024-08-17 Accepted:2024-11-07 Online:2025-03-25 Published:2025-03-25
  • Contact: GAO JianChang

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Abstract:

【Objective】 Adventitious root helps expanding root system and enhancing resistance, and its induction is widely used in asexual propagation of crops. Comparisons of the differentially expressed genes associated with adventitious root formation in different species, and analyze the conserved genes among them, so as to provide candidate genes for the comprehensive understanding of the regulatory mechanism of adventitious root formation. 【Method】 Based on the transcriptomes of adventitious root formation of Petunia hybrida, Dianthus caryophyllus, Cucumis sativus, Populus euramericana, and Fagopyrum esculentum that downloaded from the public database, we obtained transcript abundance via HISAT2 and Cufflinks pipeline, and counted and screened the differentially expressed genes by DESeq2. The homologs most similar to Arabidopsis and differentially expressed genes in each species were obtained by homologous alignment. The genes in the intersection set were obtained by set analysis, and their functional annotation and enrichment analysis were carried out in AmiGO. And qPCR was used to examine the expression patterns related to adventitious root development in crops other than these five species.【Result】 A total number of 15 conserved up-regulated genes were obtained from five species, which were mainly participate in stress response, cell division, peroxidase and mevalonate synthesis pathways. The conserved down-regulated genes and pathways mainly participate in the regulation of ion and chemical homeostasis. With the development of adventitious roots, two types (ⅠandⅡ) of expression patterns of up-regulated genes were seen. NRT3.1 and WRKY75 peaked at the early induction stage of 24 hours (typeⅠ), at the period of the adventitious root primordium formation. While the expression levels of CYCB2;4 and KNOLLE increased gradually in the later induction stage of 48-96 hours and extending to the elongation stage (typeⅡ), at the period of the adventitious root protruding beyond the periderm. Consistent patterns of the expression levels of conserved genes during the induction of adventitious roots were identified in tomatoes and watermelons, which belong to dicotyledon. While in monocotyledon like maizes, genes with higher similarity, such as WRKY75, CYCB2;4, and KNOLLE, performed similar patteren, except for NRT3.1. 【Conclusion】 Regardless of various species, tissues, and treatments, the adventitious root formation relies on the conserved pathways and genes involved in stress response and cell division. The conserved up-regulated genes NRT3.1, WRKY75, CYCB2;4, KNOLLE can be used as candidate genes for adventitious root formation for in-depth analysis in many dicotyledonous species.

Key words: adventitious root formation, adventitious root induction, cross species transcriptome, conserved genes analysis, monocotyledon, dicotyledon

Table 1

Experimental and data information of species used for comparative transcriptome analysis"

物种
Species		 组织
Tissue		 培养体系
Cultivation system		 时间点
Time point		 数据编号
Accession No.		 来源
Source
矮牵牛 P. hybrida 茎基 Stem base 基质扦插 Substrate cuttage 2 h, 6 h, 72 h, 192 h GSE57752 [6]
康乃馨 D. caryophyllus 茎基 Stem base 水培扦插 Hydroponic cuttage 6 h, 24 h, 54 h PRJEB9778 [7]
黄瓜 C. sativus 下胚轴 Hypocotyl 水淹 Water-logging 48 h PRJNA328916 [8]
欧美杨 P. euramericana 茎基 Stem base 培养基扦插 Medium cuttage 2 d, 4 d, 6 d, 8 d PRJNA516245 [9]
荞麦 F. esculentum 下胚轴外植体 Hypocotyl explants 含IAA培养基 Medium with IAA 6 h, 24 h PRJNA595876 [10]

Fig. 1

Sketch map of conserved genes analysis"

Table 2

Primers for real-time fluorescent quantitative PCR of AR conserved genes in tomato, watermelon, and maize"

基因 Gene 基因序列号 Gene ID 正向引物 Forward primer (5′-3′) 反向引物 Reverse primer (5′-3′)
SlNRT3.1 Solyc03g112100.2.1 TTAGTACTCGTGCTATTTTCGTGGC GACGATTTGTATGGCACCGTTGC
SlWRKY75 Solyc05g015850.2.1 GTCTCATCACGATGGATATGTTTCAT CCTTGTTTGAAAAGCATATCTTGGTT
SlCYCB2;4 Solyc04g082430.2.1 CATCGTCCAATCACAAGGAAGTTAG CACAATTGACCAATCTTCTGCATCT
SlKNOLLE Solyc06g053760.2.1 CAATTCAGGAGCATGGTAGGGG GGGGATAATGACTACCAGGATGAG
SlUFC1 Solyc04g076890.2.1 ACAGCGGCTGAAGGAAGAATAC ATCTGGGGCAATTCTTTGCC
ClNRT3.1 ClG42_03g0031100.10 GGGATTCTCTCATGGAAATGTCCAT TCCACTCAAACTTTTGAACCGTCTT
ClWRKY75 ClG42_07g0155600.10 GTTTTACACAGCCACCACCCG CTTCTTCTCCAACCCATCTACTCC
ClCYCB2;4 ClG42_11g0205100.10 CCACCGACCCACTTCCAGAC GAAGCGCAATACCCAGATCGT
ClKNOLLE ClG42_04g0056600.10 GGCAGCCATGAAAGATCTCG GATCGTATTACGAAGCGATTTGAG
ClRPB3 ClG42_11g0111300.10 CCGGGAACTCCGAGATGATTAC GCAAGCATCACAGTCGCGAG
ZmNRT3.1 Zm00001eb007610_T001 TAAAAGACATCACCGAGTACTTCCAC GAGTCGTTCTCCCTTCGTTGTCC
ZmWRKY75 Zm00001eb353670_T001 TTCGCGTTCCAGACGCG AGGAGTTGATTAGTGCAAGACTGGA
ZmCYCB2;4 Zm00001eb429190_T001 GCTCACGGACATCAAGAACCTCG CATATTCTGTTGCTGCAAGCGGG
ZmKNOLLE Zm00001eb056410_T001 CTTCATGAGCTACGTCGACCTGAAG GGAGGGCGTCCACCTGGC
ZmEIF5A Zm00001eb148180_T001 GCATCACCATGAAGAACTCACATCT ATCAGCTGGGATGCAGCCTGTA

Table 3

Differentially expressed gene sets and enriched items of five species"

物种
<BOLD>S</BOLD>pecies		 分析样本
Analysis samples		 上调
Up-
regulated		 下调
Down-
regulated		 上调基因显著富集GO条目
Significant GO enrichment items of
up-regulated gene set		 下调基因显著富集GO条目
Significant GO enrichment items of
down-regulated gene set
矮牵牛
P. hybrida		 72 h vs. 0 h 1757 2777 响应无机物，转录负调控，响应水缺乏，免疫应答，细胞周期
Response to inorganic substance (GO:0010035),
Negative regulation of transcription, DNA- templated (GO:0045892), Response to water deprivation (GO:0009414), Immune response (GO:0006955), Cell cycle (GO:0007049)		 光合作用，响应光照，碳水化合物合成，多糖代谢
Photosynthesis (GO:0015979), Response to light stimulus (GO:0009416), Carbohydrate biosynthetic process (GO:0016051), Polysaccharide metabolic process (GO:0005976)
康乃馨
D. caryophyllus		 54 h vs. 0 h 2638 2679 响应光照，响应温度，光合作用，响应无机物
Response to light stimulus (GO:0009416), Response to temperature stimulus (GO:0009266), Photosynthesis (GO:0015979), Response to inorganic substance (GO:0010035)		 响应光照，响应温度，响应创伤，响应脱落酸
Response to light stimulus (GO:0009416), Response to temperature stimulus (GO:0009266), Response to wounding (GO:0009611), Response to abscisic acid (GO:0009737)
黄瓜
C. sativus		 48 h vs 0 h 862 632 响应缺氧，激素介导的信号途径，响应乙烯，响应创伤，响应脱落酸
Response to hypoxia (GO:0001666), Hormone- mediated signaling pathway (GO:0009755), Response to ethylene (GO:0009723), Response to wounding (GO:0009611), Response to abscisic acid (GO:0009737)		 响应光照，响应温度，光合作用，响应无机物
Response to light stimulus (GO:0009416), Response to temperature stimulus (GO:0009266), Photosynthesis (GO:0015979), Response to inorganic substance (GO:0010035)
欧美杨
P. euramericana		 48 h vs 0 h 2539 2527 羧酸代谢，小分子生物合成，响应无机物，响应缺氧，有机环状化合物合成
Carboxylic acid metabolic process (GO:0019752),
Small molecule biosynthetic process (GO:0044283), Response to inorganic substance (GO:0010035), Response to hypoxia (GO:0001666), Organic cyclic compound biosynthetic process (GO:1901362)		 激素介导的信号途径，细胞壁重组和合成，响应几丁质，响应脱落酸，蛋白质磷酸化
Hormone-mediated signaling pathway (GO:0009755), Cell wall organization or biogenesis (GO:0071554), Response to chitin (GO:0010200), Response to abscisic acid (GO:0009737), Protein phosphorylation (GO:0006468)
荞麦
F. esculentum		 24 h vs. 0 h 3882 4826 细胞周期，细胞分裂，有机环状化合物合成，植物器官发育，结构形态发生
Cell cycle (GO:0007049), Cell division (GO: 0051301), Organic cyclic compound biosynthetic process (GO:1901362), Plant organ development (GO:0099402), Anatomical structure morphogenesis (GO:00096532)		 光合作用，响应温度，响应光照，响应无机物
Photosynthesis (GO:0015979), Response to temperature stimulus (GO:0009266), Response to light stimulus (GO:0009416), Response to inorganic substance (GO:0010035)

Fig. 2

Venn diagrams of up-regulated（left）and down-regulated（right）gene sets"

Table 4

Conserved genes and pathways"

5个物种共有上调基因
Conserved up-regulated genes of five species
拟南芥同源
Arabidopsis homolog		 功能注释
Function annotation		 矮牵牛
P. hybrida		 康乃馨
D. caryophyllus		 黄瓜
C. sativus		 欧美杨
P. euramericana		 荞麦
F. esculentum
AT1G08560.1
KNOLLE		 突触融合蛋白类蛋白（膜定位）
Syntaxin-related protein (membrane-located)		 GO_drpoolB-CL8212Contig1 Dca493 Csa4M192200 Potri.019G030800 tr_5628
AT1G22380.1
UGT85A3		 UDP-糖基转移酶
UDP-glycosyltransferase		 SG_SGN-U210923, cn7701 Dca32668 Csa3M889760, Csa5M196570 Potri.016G020900, Potri.016G105400 tr_22583
AT1G72210.1
bHLH96		 bHLH类转录因子（核定位）
Transcription factor bHLH (nucleus-located)		 GO_dr004P0004L09_F_ab1 Dca27554, Dca62583 Csa1M570740 Potri.005G071100, Potri.007G097600 tr_19165
AT1G76310.1
CYCB2;4		 细胞周期蛋白
Cyclin		 GO_dr001P0020K12_F_ab1 Dca10052, Dca44193 Csa4M658580 Potri.002G010000, Potri.009G165800 tr_227
AT1G76490.1
HMGR1		 3-羟基-3-甲基戊二酰辅酶A还原酶（内质网膜定位）
3-hydroxy-3-methylglutaryl-coenzyme A reductase (ER-membrane located)		 GO_drpoolB-CL1908Contig1, GO_drs31P0005E08_R_ab1, SG_SGN-U211455, cn6794 Dca47843 Csa7M029390 Potri.009G169900, Potri.011G145000 tr_20039, tr_14441
AT2G38870.1
PI		 蛋白酶抑制子（细胞质定位）
Protease inhibito (cytosol-located)		 cn6384, cn6635 Dca48286, Dca9747 Csa3M142910, Csa5M285030, Csa5M027950 Potri.006G212000, Potri.016G078800, Potri.016G079100, Potri.T083400 tr_7136, tr_17033, tr_17679, tr_17678, tr_2447, tr_1043
AT3G20150.1
KIN12F		 驱动蛋白样蛋白（微管定位）
Kinesin-like protein
(microtubule-located)		 cn8687 Dca24841, Dca42277 Csa3M062600 Potri.001G360200 tr_8600
AT3G26040.1
AT		 HXXXD型乙酰转移酶
HXXXD-type acyl-transferase family protein		 GO_dr001P0012O21_F_ab1, GO_dr001P0019J23_F_ab1, GO_dr004P0003P05_F_ab1 Dca38473, Dca41006 Csa4M016450, Csa1M044900, Csa6M088700 Potri.008G180400, Potri.010G056300 tr_990
AT4G02340.1
HL		 水解酶（过氧化物酶体定位）
Hydrolase (peroxisome-located)		 GO_dr001P0013L07_F_ab1 Dca30845, Dca38840, Dca42844, Dca46629, Dca49014, Dca55594 Csa4M001920 Potri.002G202700, Potri.013G134900, Potri.T121600, Potri.T121700 tr_15751, tr_26600
AT5G05340.1
PER		 过氧化物酶（外泌）
Peroxidase (secreted)		 GO_drpoolB-CL2451Contig1, GO_drpoolB-CL7003Contig1, cn2976, cn8344, cn983, cn984 Dca21353, Dca21355, Dca3360, Dca46385, Dca5472 Csa7M049140, Csa6M213910, Csa6M013940 Potri.010G236900, Potri.013G083600, Potri.013G154400, Potri.014G143200, Potri.016G132700, Potri.T163200 tr_5055, tr_5053, tr_5612, tr_8218, tr_22676, tr_11166, tr_27995, tr_4319, tr_18916
AT5G13080.1
WRKY75		 WRKY类转录因子（核定位）
Probable WRKY transcription factor (nucleus-located)		 IP_PHBS002E19u Dca5929 Csa4M012390 Potri.001G058800, Potri.001G328000, Potri.003G169100, Potri.012G101000, Potri.015G099200, Potri.T043800 tr_16853
AT5G24090.1
CHIT		 酸性内切酶（外泌）
Acidic endochitinase (secreted)		 GO_dr004P0005E08_F_ab1, cn3802 Dca5263, Dca5267 Csa5M139730 Potri.012G033900, Potri.015G024000, Potri.015G024200 tr_20433, tr_26990
AT5G47770.1
FPPS		 FPP合成酶（线粒体定位）
Farnesyl pyrophosphate synthase
(mitochondrion-located)		 GO_drpoolB-CL465Contig1 Dca41147, Dca46147 Csa6M017060 Potri.006G003400 tr_19042, tr_16531, tr_24570
AT5G50200.3
NRT3.1		 高亲和力硝酸盐转运蛋白（膜定位）
High-affinity nitrate transporter
(membrane-located)		 GO_drpoolB-CL2981Contig1 Dca23627 Csa1M047430 Potri.015G085000, Potri.015G085100 tr_15294
AT5G66230.1
CHI		 查尔酮-类黄酮易异构酶
Chalcone-flavonone isomerase		 GO_drpoolB-CL5208Contig1 Dca39417, Dca61062 Csa3M002810 Potri.005G114100, Potri.007G057800 tr_20373
5个物种和任意4个物种共有上调基因的GO富集条目
Conserved up-regulated GO enrichment items of five and any four species
路径名称
Pathway name 		路径编号
Pathway No.		 富集倍数
Fold enrichment		 校正P值
Adjusted P value
甲羟戊酸途径Isopentenyl diphosphate biosynthetic process, mevalonate GO:0019287 >100 0.02
细胞分裂Cell division GO:0051301 6.62 0.03
响应外部刺激Response to external stimulus GO:0009605 3.14 0.01
响应化学物质Response to chemical GO:0042221 2.45 0.03
响应胁迫Response to stress GO:0006950 2.34 0.01
响应刺激Response to stimulus GO:0050896 1.97 0.00
5个物种共有下调基因
Conserved down-regulated genes of five species
拟南芥同源Arabidopsis homolog 功能注释
Function annotation		 矮牵牛
P. hybrida		 康乃馨
D. caryophyllus		 黄瓜
C. sativus		 欧美杨
P. euramericana		 荞麦
F. esculentum
AT1G47670.1
AATL		 赖氨酸组氨酸转运蛋白（膜定位）
Lysine histidine transporter-like
(Membrane-located)		 GO_drpoolB-CL6245Contig1 Dca60793 Csa4M638420 Potri.014G036500 tr_13835, tr_21660
AT2G38090.1
HLP		 类同源异型域蛋白（核定位）
Homeodomain-like superfamily protein (Nucleus-located)		 GO_drpoolB-CL6570Contig1, GO_drpoolB-CL6754Contig1, GO_drs13P0026H12_F_ab1 Dca186 Csa3M732480 Potri.001G248800 tr_19808
5个物种和任意4个物种共有下调基因的GO富集条目
Conserved down-regulated GO enrichment items of five and any four species
路径名称
Pathway name		 路径编号
Pathway No.		 富集倍数
Fold enrichment		 校正P值
Adjusted P value
金属离子稳态Metal ion homeostasis GO:0055065 12.09 0.01
阳离子稳态Cation homeostasis GO:0055080 9.90 0.02
无机离子稳态Inorganic ion homeostasis GO:0098771 9.43 0.03
化学稳态Chemical homeostasis GO:0048878 7.22 0.05

Fig. 3

Expression patterns of conserved genes in P. hybrida (A), D. caryophyllus (B), and F. euramericana (C) during adventitious root formation process HPE: Hours post exposure; DAE: Days after exposure"

Fig. 4

Phynotypic changes of adventitious root formation in tomato (upper), watermelon (middle), and maize (lower) and the expression patterns of conserved genes during adventitious root formation process Bar=2 cm"

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