14-3-3蛋程中的互作靶蛋白鉴定及其对外源激素的响应

doi:10.3864/j.issn.0578-1752.2021.12.004

Abstract

Abstract:

【Objective】Grain yield and quality of rice mainly depend on grain filling. The family of 14-3-3 proteins is the important regulator of signaling in plant, and plays an important role in plant growth and development. This study was performed to assess the gene expression pattern and to identify client proteins, which would result in important information toward understanding the functional mechanism of 14-3-3 protein during rice grain filling. 【Method】 The expression pattern of each 14-3-3 genes at different grain filling stages were examined by the Real-time RT-PCR (qRT-PCR), and the family members GF14b and GF14e were used for subsequent functional analysis. The function motif of GF14b and GF14e protein were analyzed by using the KEGG database. The amplified open reading frames of GF14b and GF14e were cloned into the PGEX-6P-1 expression vector for production of the N-terminal-tagged fusion proteins GST-GF14b and GST-GF14e. The client proteins of GF14b and GF14e were captured with the affinity chromatography approach and identified by the LC-MS/MS. The protein interaction between client proteins and GF14b and GF14e were validated by the GST Pull-down in vitro. Phosphorylation sites and functions of all client proteins were analyzed using the KinasePhos online website and MapMan software (Version 3.60), respectively. The exogenous hormones (25×10 ^-6mol·L^-1 ABA,10×10^-6mol·L^-1 IAA,100×10^-6mol·L^-1 GA,50×10^-6mol·L^-1 ZR and 2×10^-4mol·L^-1 BR ) were sprayed on rice grains at 15 days after flowering to investigate the effects of exogenous hormones treatment on the expression of GF14b, GF14e and their interacting genes. 【Result】 Except for the GF14h, the remaining seven 14-3-3 family genes were expressed in rice grains, and the expression of GF14b and GF14e was high and highly variable during grain filling. Two same protein motifs and three differential motifs between GF14b and GF14e were identified with the protein sequence analysis. In total, 59 GF14b- and 72 GF14e-client proteins in rice grains were captured by affinity chromatography on a glutathione-agarose affinity column. Two randomly selected proteins from these client proteins, namely SUS3 and PSA, were further validated by GST Pull-down in vitro, and the results showed that the SUS3 interacted with GF14b and GF14e, whereas PSA specially interacted with GF14e, which confirmed the accuracy of the affinity chromatography assay. Among these client proteins, fourth-three were commonly affinity-identified by the GF14b and GF14e and were predicted to be implicated in the sucrose conversion, starch synthesis, glycolysis and TCA cycle. Meanwhile, it was found GF14b specifically bounded to the nucleotide metabolism and transporters, whilst GF14e tended to interact with the proteins involving C1 metabolism. In addition, most of the identified client proteins possess the phosphorylation sites of Ser or Thr. The present results also showed that the expression of GF14b and GF14e were up-regulated and most of the starch synthesis-related interacting genes (SUS2, AGPS, AGPL, PPDK2, SBE) were down-regulated after exogenous hormones treatment. 【Conclusion】 The magnitude of change in gene expression was greater in GF14b and GF14e than the other 14-3-3 gene family members during grain filling. The GF14b and GF14e could respond the change of hormones concentration and act as a regulator to negatively regulate the expression of starch synthesis related genes through protein-protein interaction, in turn, play an important role in starch synthesis during the grain filling stage.

Key words: rice, grain filling, 14-3-3 protein, protein-protein interactions, hormone

ZHANG ZhiXing,MIN XiuMei,SONG Guo,CHEN Hua,XU HaiLong,LIN WenXiong. Identification of 14-3-3 Client Proteins in Rice Grains and Their Response to Exogenous Hormones During the Grain Filling Stage[J].Scientia Agricultura Sinica, 2021, 54(12): 2523-2537.

Figures/Tables 9

Table 1

Fig. 1

Table 2

Fig. 2

Table 3

14-3-3 species GF14b and GF14e client proteins in developing rice grains"

登入号 Accession number^a	蛋白名称 Protein name	细胞定位 Localization^b	预测的磷酸化位点 Predicted phosphorylated site^c		互作结合 Interaction with^d
登入号 Accession number^a	蛋白名称 Protein name	细胞定位 Localization^b	Serine (S)	Threonine (T)	GF14b	GF14e
01 Sugar conversion and starch synthesis
LOC_Os01g44220	ADP-glucose pyrophosphorylase large subunit (AGPL)	Chloroplast	0	1	id	id
LOC_Os03g28330	Sucrose synthase 1 (SUS1)	Cytoplasm	5	4	id	id
LOC_Os06g09450	Sucrose synthase 2 (SUS2)	Chloroplast	3	4	id	id
LOC_Os07g42490	Sucrose synthase 3 (SUS3)	Chloroplast	5	5	id	id
LOC_Os05g33570	Pyruvate, phosphate dikinase 1 (PPDK1)	Chloroplast	5	4	id	id
LOC_Os03g31750	Pyruvate, phosphate dikinase 2 (PPDK2)	Cytoplasm	7	3	id	id
LOC_Os03g55090	Alpha-1,4 glucan phosphorylase (GP)	Cytoplasm	12	3	id	id
LOC_Os06g51084	1,4-alpha-glucan-branching enzyme (GBE)	Chloroplast	12	3	id	id
LOC_Os02g32660	Starch branching enzyme (SBE)	Chloroplast.	9	2	id	id
LOC_Os08g25734	Glucose-1-phosphate adenylyltransferase small subunit (AGPS)	Chloroplast	7	1	id	id
02 Photosynthesis
LOC_Os01g31690	Oxygen-evolving enhancer protein 1 (OEE1)	Chloroplast	3	0	id	id
LOC_Os07g04840	PsbP (PSBP)	Chloroplast	2	0	id
LOC_Os12g19470	Ribulose bisphosphate carboxylase small chain (RBCS)	Chloroplast	4	1	id
LOC_Os10g21268	Ribulose bisphosphate carboxylase large chain (RBCL)	Cytoplasm	1	1	id	id
LOC_Os12g10580	Ribulose bisphosphate carboxylase large chain (RBCL)	Chloroplast	4	2		id
LOC_Os06g04270	Putative transketolase (TK)	Chloroplast	7	4		id
03 Glycolysis
LOC_Os01g67860	Fructose-bisphosphate aldolase (FBA)	Cytoplasm	4	1	id	id
LOC_Os08g02120	Fructokinase-2 (FRK2)	Cytoplasm	0	1	id	id
LOC_Os05g33380	Fructose-bisphosphate aldolase cytoplasmic isozyme (FBA)	Cytoplasm	3	2	id	id
LOC_Os03g03720	Glyceraldehyde-3-phosphate dehydrogenase (GAPDH)	Mitochondrion	0	0		id
LOC_Os08g03290	Glyceraldehyde-3-phosphate dehydrogenase 1 (GAPDH1)	Mitochondrion	2	2	id	id
LOC_Os04g40950	Glyceraldehyde-3-phosphate dehydrogenase 2 (GAPDH2)	Mitochondrion	0	2	id	id
LOC_Os02g38920	Glyceraldehyde-3-phosphate dehydrogenase 3 (GAPDH3)	Cytoplasm	0	2	id	id
LOC_Os03g50480	Phosphoglucomutase (PGM)	Chloroplast	8	3	id	id
LOC_Os06g45710	Phosphoglycerate kinase (PGK)	Cytoplasm	3	3	id	id
LOC_Os02g07260	Phosphoglycerate kinase (PGK)	Mitochondrion	3	4	id	id
LOC_Os05g41640	Phosphoglycerate kinase (PGK)	Chloroplast	3	1	id	id
LOC_Os09g38030	UDP-glucose pyrophosphorylase (UGP)	Cytoplasm	3	6	id	id
LOC_Os02g02560	UTP--glucose-1-phosphate uridylyltransferase (UGPU)	Cytoplasm	5	3		id
04 Amino acid metabolism
LOC_Os01g55540	Aspartate aminotransferase (ASAT)	Mitochondrion	2	2	id	id
LOC_Os02g14110	Aspartate aminotransferase (ASAT)	Chloroplast	1	1		id
LOC_Os10g25130	Alanine aminotransferase (ALAT)	Cytoplasm	2	2	id	id
LOC_Os12g42876	5-methyltetrahydropteroyltriglutamate--homocysteine methyltransferase 1 (MLG1)	Chloroplast	6	1	id	id
登入号 Accession number^a	蛋白名称 Protein name	细胞定位 Localization^b	预测的磷酸化位点 Predicted phosphorylated site^c		互作结合 Interaction with^d
登入号 Accession number^a	蛋白名称 Protein name	细胞定位 Localization^b	Serine (S)	Threonine (T)	GF14b	GF14e
LOC_Os04g55720	D-3-phosphoglycerate dehydrogenase (PGDH)	Chloroplast	5	2		id
LOC_Os08g09250	Lactoylglutathione lyase (GLX-I)	Cytoplasm	0	1		id
05 nucleotide metabolism
LOC_Os10g41410	Nucleoside diphosphate kinase (NDK)	Chloroplast			id
06 TCA
LOC_Os10g33800	Malate dehydrogenase (MDH)	Cytoplasm	3	1	id	id
LOC_Os08g09200	Aconitate hydratase protein (AHP)	Chloroplast	5	0		id
07 Fermentation
LOC_Os08g43190	Sorbitol dehydrogenase (SDH)	Cytoplasm	4	1	id	id
08 Protein synthesis
LOC_Os02g32030	Elongation factor (EF)	Nucleus	10	2	id	id
LOC_Os01g53900	Elongation factor (EF)	Cytoplasm	4	5		id
LOC_Os04g02820	Elongation factor (EF)	Nucleus	10	2		id
LOC_Os03g08010	Elongation factor 1-alpha (EFA1)	Cytoplasm	2	2	id	id
LOC_Os06g37440	Elongation factor 1-gamma 3 (EFG3)	Chloroplast			id
LOC_Os11g21990	Expressed protein (EP)	Nucleus	2	3		id
LOC_Os06g48750	DEAD-box ATP-dependent RNA helicase (DEAD)	Nucleus			id
LOC_Os01g13430	Importin-alpha re-exporter (IAE)	Cytoplasm	30	8		id
LOC_Os09g07510	HEAT repeat family protein (HR)	Cytoplasm	9	2		id
LOC_Os08g39140	Heat shock protein 81-1 (HSP81-1)	Cytoplasm	5	3	id	id
LOC_Os09g30412	Heat shock protein 81-2 (HSP81-2)	Cytoplasm	2	2	id	id
LOC_Os08g06100	O-methyltransferase 1 (ROMT-9)	Cytoplasm	0	2	id	id
LOC_Os07g42950	40S ribosomal protein S6 (RPS6)	Cytoplasm	6	5		id
LOC_Os02g01280	T-complex protein (TCP)	Chloroplast	6	4		id
LOC_Os06g02380	T-complex protein (TCP)	Chloroplast	9	3		id
LOC_Os03g64210	T-complex protein (TCP)	Chloroplast	0	0	id	id
09 Transporters
LOC_Os02g10800	Mitochondrial carrier protein (MCP)	Chloroplast	2	2	id
LOC_Os01g25065	Putative ATPase beta subunit (ATPG)	Mitochondrion	3	2	id
LOC_Os11g47970	AAA-type ATPase family protein (AAA)	Cytoplasm	3	4	id
10 Disease and defense
LOC_Os11g47760	DnaK family protein (DNAK)	Cytoplasm	6	7	id	id
LOC_Os12g14070	DnaK family protein (DNAK)	Chloroplast	7	8	id	id
LOC_Os03g16860	DnaK family protein (DNAK)	Cytoplasm	6	5		id
LOC_Os02g02410	DnaK family protein (DNAK)	Mitochondrion	12	8	id	id
LOC_Os08g09770	DnaK family protein (DNAK)	Mitochondrion	6	7	id
LOC_Os11g09280	Protein disulfide isomerase-like 1-1 (PDIL1-1)	Endoplasmic reticulum	3	3	id
登入号 Accession number^a	蛋白名称 Protein name	细胞定位 Localization^b	预测的磷酸化位点 Predicted phosphorylated site^c		互作结合 Interaction with^d
登入号 Accession number^a	蛋白名称 Protein name	细胞定位 Localization^b	Serine (S)	Threonine (T)	GF14b	GF14e
11 Signal transduction
LOC_Os02g36974	14-3-3-like protein GF14-e (GF14e)	Cytoplasm	5	2	id	id
LOC_Os03g50290	14-3-3-like protein GF14-f (GF14f)	Cytoplasm	2	0	id	id
LOC_Os04g38870	14-3-3-like protein GF14-b (GF14b)	Cytoplasm	6	2	id	id
LOC_Os08g33370	14-3-3-like protein GF14-c (GF14c)	Cytoplasm	2	1	id	id
LOC_Os08g37490	14-3-3-like protein GF14-a (GF14a)	Cytoplasm	2	0	id	id
LOC_Os11g34450	14-3-3-like protein GF14-d (GF14d)	Cytoplasm	5	1		id
12 Cell growth and division
LOC_Os02g12650	Puromycin-sensitive aminopeptidase (PSA)	Cytoplasm	6	2		id
LOC_Os08g30810	Puromycin-sensitive aminopeptidase (PSA)	Cytoplasm	5	4		id
LOC_Os02g02890	Peptidyl-prolyl cis-trans isomerase (CYP2)	Mitochondrion	3	4	id
LOC_Os01g59790	ADP-ribosylation factor 1 (ARF1)	Mitochondrion	0	0	id
LOC_Os03g51600	Tubulin alpha-1 chain (TUBA1)	Mitochondrion	6	1	id
LOC_Os05g34170	Tubulin beta-6 chain (TUBB6)	Cytoplasm	6	2	id	id
LOC_Os06g46000	Tubulin beta-3 chain (TUBB3)	Cytoplasm	5	3		id
LOC_Os11g14220	Tubulin alpha-2 chain (TUBA2)	Cytoplasm	7	1		id
LOC_Os12g44350	Actin-1 (ACTIN1)	Cytoplasm	2	3		id
LOC_Os03g50885	Actin-1 (ACTIN1)	Cytoplasm	4	2	id
LOC_Os11g06390	Actin-7 (ACTIN7)	Cytoplasm	7	2		id
LOC_Os10g36650	Actin-2 (ACTIN2)	Cytoplasm	7	2		id
LOC_Os01g73310	Putative actin (ACTIN)	Cytoplasm	5	2		id
LOC_Os05g01600	Actin-97(ACTIN97)	Cytoplasm	5	2		id
13 C1-metabolism
LOC_Os09g27420	Formate--tetrahydrofolate ligase (FTL)	Chloroplast	10	5		id
LOC_Os06g29180	Formate dehydrogenase 1 (FDH1)	Mitochondrion	0	3		id
14 Unknown classification
LOC_Os03g49190	Oleosin 18 kDa (OLE18)	Cytoplasm	1	0	id
LOC_Os06g49650	Harpin-induced protein 1 domain containing (HIP1)	Nucleus	3	1	id

Table 3

Fig. 3

Fig. 4

Fig. 5

Fig. 6

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基因 Gene	Accession No.	正向引物序列 Forward primer sequence (5′-3′)	反向引物序列 Reverse primer sequence (5′-3′)
Primer for qRT-PCR
GF14a	LOC_Os08g37490	AGCCATGAAGGAGCTGTCGC	GCTCATCCTCAGGCTTGGTT
GF14b	LOC_Os04g38870	GCTTGAATCCCACCTTGTC	AATGTCCTGAGCAGCCTTG
GF14c	LOC_Os08g33370	CGTTTGACGAAGCCATCTCC	CTAGTAGAACAGGAGAAGAATC
GF14d	LOC_Os11g34450	TGCTCTCGCAGATTTGGCTC	ATCCCCAGGCTCTTTTGGAG
GF14e	LOC_Os02g36974	GATATTGCCCTGGCAGAGTTG	GAGATATCGGAAGTCCACAGC
GF14f	LOC_Os03g50290	AGCAGCTGAGAACACTCTTG	CAGCAATAGCATCGTCGAAC
GF14g	LOC_Os01g11110	AGCGACGACCTCGTCTACAT	TGACTCTCCTTGCCCTTTGT
GF14h	LOC_Os11g39540	TTATGGCCTATCAGGCTTGG	TTCTCCTTCAGGAGCTGCAT
AGPS	LOC_Os08g25734	TTACTGGGAAGACATTGGTACC	CTCCCATGAGTAATGAGTCCTC
AGPL	LOC_Os01g44220	GGAAAGATTGAATATTGGGGGC	TCAGAGGAAAGAGTTGAACTCC
SBE	LOC_Os02g32660	GATCAGTATGAAGGAGGACTGG	ACCTACTAATGCTGCAGAATGT
SUS2	LOC_Os06g09450	GGAGAAAACCAAATACCCCAAC	CAGTGTGATTCATGGCGATAAG
PPDK2	LOC_Os03g31750	CTAGCGGAATTCTTCTCGTTTG	CAAATGCCCACCTCTAAATCAG
β-actin	LOC_4333919	CTGCGGGTATCCATGAGACT	GCAATGCCAGGGAACATAGT
Primer for PCR
GF14b	LOC_Os04g38870	TTTTTTGGATTCATGTCGGCACAGGCGGAGCTTTCC	TATATATACTCGAGCTGCCCCTCGCTGGAGTCGCGCTT
GF14e	LOC_Os02g36974	TTTCGAATTCATGTCGCAGCCTGCTGAGCTTTCCC	TTTCTCGAGCTGTCCATCTCCTGATTCGCCCTTGT
SUS3	LOC_Os07g42490	TCCGAATTCATGGGGGAAACTACTGGAGAACGTGC	TTTTCTCGAGTTTGGTGGAGGCCTCTCCCTCAATG
PSA	LOC_Os02g12650	GGGGGGGAATTCATGCATGGCTTCTACAGAAGTGTG	GAGCTCGAGGTGGTCGTGAGAAATTTCCTTGAGGAC

功能位点 Functional site	功能位点位置 Functional site location
功能位点 Functional site	GF14b	GF14e
pf:IFT20	5-55
pf:DUF885	16-149	6-150
pf:14-3-3	9-245	9-245
pf:TPR_12	135-207	135-207
pf:FlaF		192-254

Identification of 14-3-3 Client Proteins in Rice Grains and Their Response to Exogenous Hormones During the Grain Filling Stage

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