CclSAUR49 Affects Growth and Limonoids Metabolism in Citrus

doi:10.16420/j.issn.0513-353x.2023-0117

Acta Horticulturae Sinica ›› 2024, Vol. 51 ›› Issue (3): 479-494.doi: 10.16420/j.issn.0513-353x.2023-0117

• Genetic & Breeding·Germplasm Resources·Molecular Biology • Previous Articles Next Articles

CclSAUR49 Affects Growth and Limonoids Metabolism in Citrus

YI Qian, ZHANG Manman, WANG Xiaoli, FENG Jipeng, ZHU Shiping, WANG Fusheng^*(), ZHAO Xiaochun^*()

National Citrus Engineering Research Center，Citrus Research Institute of Southwest University/Chinese Academy of Agricultural Sciences，Chongqing 400712，China

Received:2023-04-10 Revised:2023-11-21 Online:2024-03-25 Published:2024-03-22
Contact: WANG Fusheng, ZHAO Xiaochun

Abstract

Abstract:

SAUR（Small auxin up-regulated RNA） is a plant-specific early auxin response gene. In order to study the function of CclSAUR49 in regulating limonoid metabolism in citrus，six CclSAUR49 overexpression plants（OE1-OE6）and two RNA interference plants（Ri1 and Ri2）were generated through genetic transformation with epicotyl of Poncirus trifoliata Raf. The growth performance of transgenic and wild type plants was observed and compared. The epidermal microstructure and tissue structure of leaves were observed by electron microscopy and semi-thin sections，respectively. The contents of auxin and limonoids in the leaves were also detected. The morphological performance of the six overexpression plants was different. Compared with the wild type，the shoot length of OE2 increased by 23.21%，the number of internodes increased，and the leaf length increased by 17.97%. The branch growth of two RNA interference expression plants（Ri1 and Ri2）was less than 23.95% and 46.82%. The main leaf vein diameter of 2/3 overexpression plants increased，while Ri2 decreased. The expressions level of CclSAUR49 in the leaves of six overexpression plants were significantly up-regulated，which was 2.47-73.29 times of the wild type. The expression of CclSAUR49 in the leaves of two RNA interference expression plants were significantly inhibited，and the expression levels were 22.66% and 47.22% of the wild type. The expression level of CclSAUR49 in the leaves of transgenic plants was significantly positively correlated with its auxin content，and was significantly positively correlated with the expression levels of auxin biosynthesis（YUC6 and YUC10），transport（PIN3）and signal transduction（CiARF7 and CiARF9）genes in the transgenic plants. The content of limonoids in the leaves of four overexpression plants decreased，and the content of limonoids in the leaves of one RNA interference expression plant（Ri1）increased significantly. In the RNA interference expression plants，the content of limonoids was significantly negatively correlated with the content of auxin. The above results indicate that CclSAUR49 can promote the growth and development of citrus plants，and regulate the auxin level in plant tissues by affecting the expression of genes in auxin biosynthesis，transport and signal transduction pathways，thereby affecting the metabolism of limonoids.

Key words: citrus, CclSAUR49, genetic transformation, auxin, limonoids

YI Qian, ZHANG Manman, WANG Xiaoli, FENG Jipeng, ZHU Shiping, WANG Fusheng, ZHAO Xiaochun. CclSAUR49 Affects Growth and Limonoids Metabolism in Citrus[J]. Acta Horticulturae Sinica, 2024, 51(3): 479-494.

Figures/Tables 15

References 41

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引物名称 Primer name	正向引物序列（5′-3′） Forward primer sequence	反向引物序列（5′-3′） Reverse primer sequence
SAU49OE	ATTTAAATATGGCTATTCATGTACCTGGAATC	GGATCCATATGATTCATTCAAGCTGGAAGT
M13Rf	TTCACACAGGAAACAGCTATGAC
SAUR49-RNAi	TCTAGAATTTAAATATGGCTATTCATGTACCTGGAATC	GGATCCATTTAAATTCATGATTCATTCAAGCTGGAA
59MSac-F	CACGCTCGAGTATAAGAGCTCT
59MBcu1-R		GGACTAGTCCCGGGTCTTAAT
SAUR49	ACATCCACAGTTGTGCCAAAAG	CAAACCCGAATTCTTCCTCAGC
YUC1	CACAATGCAATCCCTCACATG	ACCTTAACGGAAACCACCTGA
YUC2	CGCCTTGTGGATCAATTTTTA	AATGTTGCCGCTTCTGATCTT
YUC3	TGTGTTGGACATTGGTGCTTT	ACATTGCTTCGGTACCCAGTT
YUC5	GATTACAAGTCCGGCGAAAA	TGATGGAGAGGCATTGTGGTT
YUC6	AGAGGCAAAAGGGTTTTGGTT	CGAAAGTTGATTTCCCCAGC
YUC10	GGCTTTTGAATGGGATGATGA	ATTTGATTTGATGGCCCAACT
PIN1	GGAGCTGGAGCTAGGGATCTT	CTCCTTTTCCTCCTTGTGGTG
PIN2	GAGTGGCGAGCTTTTTAACG	ACCACCACCAACACTCTCCTT
PIN3	AAAACGGGGATTTTGGTAGG	GCGGGTCCACCTTCTTTATGA
PIN5	GATGAAGCTTGTGTGGCTGAA	AATGCCACCTGTTTGACACAA
PIN6	GAAATGGACGCGGTTACTGTT	GCCAGCTTGCCTATCTCCTTG
CiARF1	CTTGTAACCCTTCCTCGTG	GAAGAACGGAGAACCCAC
CiARF2	GTCAACTAATCAGGTCGCA	GGAAGACACTCATCAGCAT
CiARF7	AGTTGGAATAGAGCGTCG	GGAAGATTTGGATAGTTTGG
CiARF9	GGATTCCGTTGTTTCGTC	AATTCCTGAGTTGGGGTT
CiARF10	TGAAGAATGAGACTCGCTA	AACCTGTTCGCTATGACC
CiARF12	ACAGCCAAGATGATAAAGC	AATTCCCAACTTCCAGACT
CiARF13	TCAGAGGATGTAGGTCGCA	CAATCTTCTAGCCGTTTTCA
CiARF18	GGTTCTAAATGGCGGTCGT	CGACGCAGGAATGTCAATG
CiOSC	CTTTTGGCCTGGTGACTATGGT	CATTTCCCTTCGATGTTCCACT
CiMYB42	GGGCGAACCGATAACGAGAT	GCTGGAGTCTGGCAGCAAAT
GAPDH	GGAAGGTCAAGATCGGAATCAA	CGTCCCTCTGCAAGATGACTCT

引物名称 Primer name	正向引物序列（5′-3′） Forward primer sequence	反向引物序列（5′-3′） Reverse primer sequence
SAU49OE	ATTTAAATATGGCTATTCATGTACCTGGAATC	GGATCCATATGATTCATTCAAGCTGGAAGT
M13Rf	TTCACACAGGAAACAGCTATGAC
SAUR49-RNAi	TCTAGAATTTAAATATGGCTATTCATGTACCTGGAATC	GGATCCATTTAAATTCATGATTCATTCAAGCTGGAA
59MSac-F	CACGCTCGAGTATAAGAGCTCT
59MBcu1-R		GGACTAGTCCCGGGTCTTAAT
SAUR49	ACATCCACAGTTGTGCCAAAAG	CAAACCCGAATTCTTCCTCAGC
YUC1	CACAATGCAATCCCTCACATG	ACCTTAACGGAAACCACCTGA
YUC2	CGCCTTGTGGATCAATTTTTA	AATGTTGCCGCTTCTGATCTT
YUC3	TGTGTTGGACATTGGTGCTTT	ACATTGCTTCGGTACCCAGTT
YUC5	GATTACAAGTCCGGCGAAAA	TGATGGAGAGGCATTGTGGTT
YUC6	AGAGGCAAAAGGGTTTTGGTT	CGAAAGTTGATTTCCCCAGC
YUC10	GGCTTTTGAATGGGATGATGA	ATTTGATTTGATGGCCCAACT
PIN1	GGAGCTGGAGCTAGGGATCTT	CTCCTTTTCCTCCTTGTGGTG
PIN2	GAGTGGCGAGCTTTTTAACG	ACCACCACCAACACTCTCCTT
PIN3	AAAACGGGGATTTTGGTAGG	GCGGGTCCACCTTCTTTATGA
PIN5	GATGAAGCTTGTGTGGCTGAA	AATGCCACCTGTTTGACACAA
PIN6	GAAATGGACGCGGTTACTGTT	GCCAGCTTGCCTATCTCCTTG
CiARF1	CTTGTAACCCTTCCTCGTG	GAAGAACGGAGAACCCAC
CiARF2	GTCAACTAATCAGGTCGCA	GGAAGACACTCATCAGCAT
CiARF7	AGTTGGAATAGAGCGTCG	GGAAGATTTGGATAGTTTGG
CiARF9	GGATTCCGTTGTTTCGTC	AATTCCTGAGTTGGGGTT
CiARF10	TGAAGAATGAGACTCGCTA	AACCTGTTCGCTATGACC
CiARF12	ACAGCCAAGATGATAAAGC	AATTCCCAACTTCCAGACT
CiARF13	TCAGAGGATGTAGGTCGCA	CAATCTTCTAGCCGTTTTCA
CiARF18	GGTTCTAAATGGCGGTCGT	CGACGCAGGAATGTCAATG
CiOSC	CTTTTGGCCTGGTGACTATGGT	CATTTCCCTTCGATGTTCCACT
CiMYB42	GGGCGAACCGATAACGAGAT	GCTGGAGTCTGGCAGCAAAT
GAPDH	GGAAGGTCAAGATCGGAATCAA	CGTCCCTCTGCAAGATGACTCT

样品 Material	叶长/mm Length of leaf	叶宽/mm Width of leaf	分枝长/mm Branch length	节间数 Number of internodes	节间长/mm Length of internode	茎粗/mm Circumference of stem
WT	33.89 ± 2.07	9.39 ± 0.96	114.81 ± 0.51	7	21.80 ± 4.80	2.74 ± 0.43
OE1	34.10 ± 3.60	10.40 ± 1.22	49.01 ± 0.49^**	6	12.25 ± 2.35^*	2.18 ± 0.33^*
OE2	39.98 ± 0.68^*	11.17 ± 0.93^*	141.46 ± 0.60^**	9	20.68 ± 4.46	2.69 ± 0.41
OE3	34.25 ± 4.39	9.23 ± 1.96	139.10 ± 0.61^**	9	21.19 ± 10.45	2.49 ± 0.23
OE4	33.35 ± 5.16	8.85 ± 0.88	111.51 ± 0.34	7	18.62 ± 3.30	2.45 ± 1.16
OE5	34.54 ± 4.47	9.54 ± 0.84	107.63 ± 0.37^**	8	16.81 ± 6.68	2.40 ± 0.13
OE6	33.43 ± 3.99	8.63 ± 1.07	93.87 ± 0.39^**	7	13.22 ± 2.47^*	1.83 ± 0.25^**
Ri1	33.39 ± 6.14	9.33 ± 0.91	87.31 ± 0.24^**	8	11.78 ± 1.79^*	2.12 ± 0.47^**
Ri2	32.19 ± 6.48	9.63 ± 0.57	61.06 ± 0.33^**	6	10.42 ± 0.55^*	2.13 ± 0.18^*

样品 Material	叶长/mm Length of leaf	叶宽/mm Width of leaf	分枝长/mm Branch length	节间数 Number of internodes	节间长/mm Length of internode	茎粗/mm Circumference of stem
WT	33.89 ± 2.07	9.39 ± 0.96	114.81 ± 0.51	7	21.80 ± 4.80	2.74 ± 0.43
OE1	34.10 ± 3.60	10.40 ± 1.22	49.01 ± 0.49^**	6	12.25 ± 2.35^*	2.18 ± 0.33^*
OE2	39.98 ± 0.68^*	11.17 ± 0.93^*	141.46 ± 0.60^**	9	20.68 ± 4.46	2.69 ± 0.41
OE3	34.25 ± 4.39	9.23 ± 1.96	139.10 ± 0.61^**	9	21.19 ± 10.45	2.49 ± 0.23
OE4	33.35 ± 5.16	8.85 ± 0.88	111.51 ± 0.34	7	18.62 ± 3.30	2.45 ± 1.16
OE5	34.54 ± 4.47	9.54 ± 0.84	107.63 ± 0.37^**	8	16.81 ± 6.68	2.40 ± 0.13
OE6	33.43 ± 3.99	8.63 ± 1.07	93.87 ± 0.39^**	7	13.22 ± 2.47^*	1.83 ± 0.25^**
Ri1	33.39 ± 6.14	9.33 ± 0.91	87.31 ± 0.24^**	8	11.78 ± 1.79^*	2.12 ± 0.47^**
Ri2	32.19 ± 6.48	9.63 ± 0.57	61.06 ± 0.33^**	6	10.42 ± 0.55^*	2.13 ± 0.18^*

材料 Material	气孔密度/（个 · mm^-2） Stomatal density	气孔长/μm Stomatal length	气孔宽/μm Stomatal width	长/宽 Length/width
WT	513.48 ± 67.48	6.89 ± 0.79	2.84 ± 0.47	2.48 ± 0.45
OE1	795.27 ± 172.92^*	8.90 ± 1.73^**	3.85 ± 0.97^*	2.47 ± 0.87
OE4	633.16 ± 43.43	9.08 ± 2.18^**	3.36 ± 0.50^*	2.80 ± 1.00
OE6	590.32 ± 197.93	8.70 ± 1.84^*	3.49 ± 0.33^*	2.51 ± 0.55
Ri1	451.17 ± 78.43	7.45 ± 0.89	3.75 ± 0.53^**	2.03 ± 0.43^*
Ri2	450.78 ± 77.64	7.50 ± 1.03	3.80 ± 0.51^**	2.01 ± 0.42^*

CclSAUR49 Affects Growth and Limonoids Metabolism in Citrus

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材料 Material	上表皮厚度/μm Upper epidermis thickness	栅栏组织厚度/μm Palisade tissue thickness	海绵组织厚度/μm Spongy tissue thickness	下表皮厚度/μm Lower epidermis thickness	叶片厚度/μm Leaf thickness
WT	109.93 ± 22.42	680.87 ± 121.61	1 466.00 ± 149.83	107.00 ± 11.25	2 338.95 ± 264.67
OE1	114.15 ± 0.73	742.36 ± 53.01	1 892.14 ± 196.81^**	98.75 ± 5.11	2 829.78 ± 222.03^**
OE2	130.01 ± 23.40	764.09 ± 13.95	1 644.52 ± 116.20^*	126.93 ± 23.11	2 683.47 ± 118.27^*
OE3	144.51 ± 22.58	771.81 ± 77.53	1 608.60 ± 124.06	138.91 ± 7.88^**	2 615.85 ± 132.88
OE4	117.77 ± 12.20	829.49 ± 60.36^*	1 469.14 ± 149.94	135.17 ± 7.50^**	2 514.08 ± 219.72^*
OE5	136.67 ± 10.69	697.89 ± 83.04	1 702.15 ± 35.11^*	121.90 ± 9.18	2 624.05 ± 107.69
OE6	150.89 ± 13.83^**	736.44 ± 21.08	1 793.58 ± 163.60^**	129.23 ± 11.49^*	2 760.68 ± 123.19^**
Ri1	115.31 ± 1.07	823.56 ± 90.64	1 402.75 ± 223.99	102.54 ± 11.72	2 376.40 ± 179.23
Ri2	111.86 ± 19.14	759.21 ± 67.45	1 386.99 ± 89.47	95.72 ± 9.63	2 344.54 ± 199.23

材料 Material	叶脉直径/μm Leaf vein diameter	栅栏组织层数 Layers	栅/海比 P/S	叶组织结构紧密度/% CTR	叶组织结构疏松度/% SR
WT	5 273.96 ± 592.91	2 ~ 3	0.47 ± 0.08	28.83 ± 0.04	62.33 ± 0.03
OE1	5 746.06 ± 850.10	2 ~ 3	0.40 ± 0.07	26.67 ± 0.04	67.00 ± 0.02^*
OE2	6 603.56 ± 222.93^**	2 ~ 3	0.47 ± 0.04	28.67 ± 0.01	61.33 ± 0.02
OE3	6 610.38 ± 314.27^**	2 ~ 3	0.49 ± 0.08	29.33 ± 0.03	61.33 ± 0.04
OE4	6 533.15 ± 150.19^**	2 ~ 3	0.57 ± 0.03^*	33.00 ± 0.02^*	58.33 ± 0.01^*
OE5	5 865.42 ± 590.89	2 ~ 3	0.41 ± 0.04	26.33 ± 0.02	65.00 ± 0.02
OE6	6 327.06 ± 397.70^*	2 ~ 3	0.41 ± 0.03	26.67 ± 0.01	65.00 ± 0.03
Ri1	5 388.89 ± 107.31	2 ~ 3	0.60 ± 0.15	35.00 ± 0.06	58.67 ± 0.05
Ri2	4 484.16 ± 32.01^*	2 ~ 3	0.54 ± 0.03	32.33 ± 0.01	59.33 ± 0.01

基因Gene	CclSAUR49	IAA
CclSAUR49	1	0.623^**
YUC6	0.649^**	0.431^*
YUC10	0.451^**	0.249
PIN3	0.873^**	0.487^**
CiARF7	0.687^**	0.618^**
CiARF9	0.529^**	0.533^**

材料 Material	指标	类柠檬苦素含量 Limonoids content	CiOSC	CiMYB42
转基因植株Transgenic plant	CclSAUR49	-0.452	-0.118	0.062
	类柠檬苦素含量Limonoids content	1	0.452	0.267
	生长素含量Auxin content	-0.661^**	/	/
过量表达植株	CclSAUR49	-0.533^*	0.049	-0.028
Overexpression transgenic plant	类柠檬苦素含量Limonoids content	1	0.077	0.680^**
	生长素含量Auxin content	-0.287	/	/
干扰表达植株RNAi transgenic plant	CclSAUR49	-0.068	-0.667^*	0.774^*
	类柠檬苦素含量Limonoids content	1	0.753	0.413
	生长素含量Auxin content	-0.775^*	/	/

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