Dynamic Changes of Auxin and Analysis of Differentially Expressed Genes in Walnut Endocarp During Hardening

doi:10.16420/j.issn.0513-353x.2020-0438

Acta Horticulturae Sinica ›› 2021, Vol. 48 ›› Issue (3): 487-504.doi: 10.16420/j.issn.0513-353x.2020-0438

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Dynamic Changes of Auxin and Analysis of Differentially Expressed Genes in Walnut Endocarp During Hardening

YU Shangqi¹^,²^,⁴, ZHANG Rui²^,³^,⁴^,^*(), GUO Zhongzhong¹^,², SONG Yan²^,³, FU Jiazhi²^,³, WU Pengyu²^,³, MA Zhihao³

¹College of Life Science,Tarim University,Alar,Xinjiang 843300,China
²Production and Construction Corps Key Laboratory of Protection and Utilization of Biological Resources in Tarim Basin,Alar,Xinjiang 843300,China
³College of Plant Science and Technology,Tarim University,Alar,Xinjiang 843300,China
⁴The National and Local Joint Engineering Laboratory of High Efficiency and Superior-Quality Cultivation and Fruit Deep Processing Technology of Characteristic Fruit Trees in South Xinjiang,Alar,Xinjiang 843300,China

Received:2020-11-16 Online:2021-03-25 Published:2021-04-02
Contact: ZHANG Rui E-mail:zhrgsh@163.com

Abstract

Abstract:

In order to study the hardening of the walnut endocarp,which mainly involves the biological process and the role of auxin in the hardening process,the‘Xinlu’walnut was used as the research material. There is a close relationship between walnut endocarp hardening and distribution of vascular bundles on the walnut endocarp surface by morphological observation and lignin deposition analysis;The hardening of walnut endocarp near the vascular tissue is earlier than that away from the vascular tissue. The content of IAA showed a V-shaped change in the hardening of the endocarp. The average content of IAA was the highest than others during the five stages,16.467 ng·g^-1,which was about 6.8 times of the sum of IBA,ICA and ME-IAA. The analysis of intermediate metabolites of lignin synthesis showed that the content of p-coumaryl alcohol of lignin monomer in the hardening area of the endocarp was 16 times of the unhardening area. The content of sinapyl alcohol in the hardening area of the walnut endocarp was extremely high,but it was not detected in the unhardening area,and the content of these two substances in the hardening area of the walnut endocarp showed an overall upward trend with the hardening process. Through transcriptome and proteome correlation analysis,369 differentially expressed genes related to endocarp hardening were obtained. The correlation result of genes that are differentially expressed at both the transcription and protein levels is good,with the lowest correlation coefficient of 0.48124,but the correlation result of all differentially expressed genes is poor,with the highest correlation coefficient of 0.22112. Using Metascape to construct a network of relationships among the top 20 biological functions that are significantly enriched by differentially expressed genes,it is found that four biological processes,namely Phenylpropanoid metabolic process,Response to oxidative stress,Cell wall organization or biogenesis,Amino sugar and nucleotide sugar metabolism were mainly involved in endocarp hardening mainly involve. The fluorescence quantitative results showed that the expression changes trend of AUX/IAA genes JrIAA9,JrIAA16 and JrIAA27 were basically consistent with that of IAA content. It is speculated that IAA plays an important regulatory role in the process of walnut endocarp hardening,and it is of great significance to carry out the research on the mechanism of Bared-nut later.

Key words: walnut, auxin, endocarp, transcriptome, proteome, correlation analysis, lignin

CLC Number:

S664.1

YU Shangqi, ZHANG Rui, GUO Zhongzhong, SONG Yan, FU Jiazhi, WU Pengyu, MA Zhihao. Dynamic Changes of Auxin and Analysis of Differentially Expressed Genes in Walnut Endocarp During Hardening[J]. Acta Horticulturae Sinica, 2021, 48(3): 487-504.

Figures/Tables 12

Table 1 The primers of qRT-PCR

引物名称	引物序列（5′-3′）	长度/bp	退火温度/℃
Primer name	Primer sequence	Length	Annealing temperature
JrIAA9-F	TCTGGGTTCATCAGCAGCACG	21	59.52
JrIAA9-R	TGCGATGCTGTCCTCAAGGT	20	57.45
JrIAA16-F	AGTGCTTGACCGCACAGGTT	20	57.45
JrIAA16-R	TGCTTGTAGGCGATGTGCCA	20	57.45
JrIAA27-F	GCTAGCACCAAGGGCAATGGA	21	59.52
JrIAA27-R	AGGGAAAGGGTGGGGCCTAAT	21	59.52
JrPAL1-F	ACAACCGGCTTCCGGTACTCCT	22	61.40
JrPAL1-R	AACGGCAACGGCAACGGCAA	20	59.50
Jr4CL1-F	ACTGTGCGTATTGCCGCTGT	20	59.52
Jr4CL1-R	TCGCCAAGACAATCGGTGGA	20	57.45
JrC4H1-F	GTTAGCCCTGTTTGTAGCCGC	21	57.45
JrC4H1-R	TTGGCCATGTCGGTGAGGTT	20	57.45
JrC3H1-F	TTGCACGTGATCCGGCAGT	19	57.32
JrC3H1-R	TGGTGCAGTAGGTGAGCAAGC	21	59.52
JrF5H1-F	TTCACAGGCTTGCCGATGCT	20	57.45
JrF5H1-R	ACATGGCCTTCGCTCACTACG	21	59.52
JrCAD1-F	ACAACACGACCTCTGCTTGTTA	22	55.81
JrCAD1-R	CGTTGTGGATGTTGCTGGAAGT	22	57.67
JrCCR1-F	TTCTGCAGCGCGGTTACACT	20	57.45
JrCCR1-R	TCACAGCCCTGAATAGCAGCA	21	57.57
JrCOMT1-F	TCTTCTCAGATCCTCGCCCGTGTC	24	62.98
JrCOMT1-R	TTCTCTCGGAGTCGGAGTCGTTGG	24	62.98
JrCCOAOMT1-F	AGCGGTATTCGGGGGTTTGGT	21	59.52
JrCCOAOMT1-R	CGTCGTGGCGCCTCCTGATG	20	63.60
JrPER1-F	TGCTTCGCTGCTGCTGGACTCAA	23	61.33
JrPER1-R	TCCCACCGCAACAATGCCATCTCT	24	61.28
JrLACC1-F	AGCTGACAGTTGTGGGTGCGGATG	24	62.98
JrLACC1-R	AGAATGGCGGTGGTGGTGGTGTTG	24	62.98
JrLTPG1-F	TGCGGTGGTGTTGGTCGCAA	20	59.50
JrLTPG1-R	AGCAACTGCTGGGTGCTTCG	20	59.50

Fig. 1 Dynamic changes of endocarp development of walnut in different days after florescence A-D:Changes of lignin accumulation in endocarp of the‘Zhipi’walnut during 37,44,66 and 80 days after florescence. E-J:Changes of lignin accumulation in endocarp of the‘Xinlu’walnut during 50,57,64,71,78 and 85 days after florescence. K-L:The form of endocarp of the‘Xinlu’walnut before ripening. M-P:The cell form of ovary wall of the‘Xinlu’walnut. Q-S:The form of endocarp of the‘Xinlu’walnut after ripening. Te:Testa;Co:Cotyledon;Ex:Exocarp;Me:Mesocarp;En:Endocarp;Pu:Pulpy;Sc:Sclerotic;Va:Vascular bundle;Iwo:Inner wall of ovary;Mwo:Middle wall of ovary;Owo:Outer wall of ovary.

Fig. 2 Endogenous hormone levels in endocarp of‘Xinlu’walnut Lower case letters indicate that the same endogenous auxin has significant difference at the 5% level.

Fig. 3 Changes of intermediate metabolites of lignin synthesis and schematic diagram of the lignin metabolism pathway X is for something else,and the arrows represent the upstream and downstream relationships of metabolite production.A:Cinnamic acid;B:L-Phenylalanine;C:p-Coumaric acid;D:Caffeic acid;E:Ferulic acid;F:Sinapic acid;G:p-Coumaraldehyde;H:Caffeyl aldehyde;I:4-Hydroxy-3-methoxycinnamaldehyde;J:Sinapinaldehyde; K:p-Coumaryl alcohol;L:Caffeyl alcohol;M:Coniferyl alcohol;N:Sinapyl alcohol; “*”means that the content of metabolite is significantly different between the two regions of endocarp during the same period, and“**”means that the content of metabolite is extremely significanly different between the two regions of endocarp during the same period. The same below.

Table 2 Association statistics of transcriptome and proteome

比对组 Group name	关联水平 Type of correlations	蛋白质数量 Number of proteins	基因数量 Number of genes	关联数量 Number of correlations
57 d-VS-71 d	鉴定Identification	6 776	75 654	6 751
	定量Quantitative	6 765	75 654	6 740
	差异表达Differentially expressed	545	8 339	110
57 d-VS-85 d	鉴定 Identification	6 776	76 053	6 756
	定量Quantitative	6 770	76 053	6 750
	差异表达Differentially expressed	1 260	9 985	300

Fig. 4 Enrichment analysis of differentially expressed genes in comparison group（57 d-VS-71 d and 57 d-VS-85 d） Bar graph of enriched terms across input gene lists, colored by p-values. The smaller the p value is,the more reliable the enriched item is,i.e. the larger the -log10 (p) value is, the more reliable the enriched item is. A1:M00138:Flavonoid biosynthesis, naringenin => pelargonidin;A2:ath00520:Amino sugar and nucleotide sugar metabolism;A3:GO:0044036:Cell wall macromolecule metabolic process;A4:GO:0009408:Response to heat;A5:GO:0019751:Polyol metabolic process;A6:GO:0017144:Drug metabolic process;A7:GO:0016052:Carbohydrate catabolic process;A8:GO:0006979:Response to oxidative stress;A9:GO:0010038:Response to metal ion;B1:ath00940:Phenylpropanoid biosynthesis;B2:GO:0046686:Response to cadmium ion;B3:GO:0017144:Drug metabolic process;B4:ath00360:Phenylalanine metabolism;B5:GO:0009266:Response to temperature stimulus;B6:GO:0071554:Cell wall organization or biogenesis;B7:ath01230:Biosynthesis of amino acids;B8:GO:0006826:Iron ion transport;B9:GO:0051186:Cofactor metabolic process;B10:GO:0009226:Nucleotide-sugar biosynthetic process;B11:GO:0009636:Response to toxic substance;B12:ath00500:Starch and sucrose metabolism;B13:GO:0006575:Cellular modified amino acid metabolic process;B14:GO:0009072:Aromatic amino acid family metabolic process;B15:GO:0006457:Protein folding;B16:M00002:Glycolysis, core module involving three-carbon compounds;B17:ath00960:Tropane, piperidine and pyridine alkaloid biosynthesis;B18:GO:0042133:Neurotransmitter metabolic process;B19:GO:0018298:Protein-chromophore linkage. B20:GO:0010431:Seed maturation.

Table 3 Correlation coefficient between mRNA expression and protein expression of the differentially expressed genes

比对组	亚组类型	斯皮尔曼相关系数（R）
Group name	Type of subgroup	Spearman correlation coefficient
57 d-VS-71 d	DEPs_DEGs	0.481 24
	DEPs_DEGs_Same Trend	0.802 57
	DEPs_DEGs_Opposite	-0.821 57
	DEPs_NDEGs	0.020 74
	NDEPs_DEGs	0.123 15
	NDEPs_NDEGs	0.045 00
	ALL	0.073 99
57 d-VS-85 d	DEPs_DEGs	0.700 65
	DEPs_DEGs_Same Trend	0.833 35
	DEPs_DEGs_Opposite	-0.573 34
	DEPs_NDEGs	0.225 70
	NDEPs_DEGs	0.356 13
	NDEPs_NDEGs	0.085 44
	ALL	0.221 12

Fig. 6 Network of the enriched function for hardening of walnut endocarp The picture shows the visual relationship network among the Terms of the clusters that were enriched the top 20 significantly. For the convenience of drawing,selected the Terms with the best P-value in each cluster,but the number of Term does not exceed 15. In 20 clusters,the total number of Term does not exceed 250. Each node represents a Term. When the member similarity between Term > 0.3,the Term is connected by edges. Different colors in Pic1 represent different clusters,and Term in the same cluster has the same color. The name of the cluster is the name of the term with the most significant statistical significance in a cluster. Different colors in Pic2 represent the conversion value of Term's P-value[Log10(P)]. The darker the color,the higher the significance of Term. A:Phenylpropanoid metabolic process;B:Response to oxidative stress;C:Cell wall organization or biogenesis;D:Response to metal ion;E:Response to temperature stimulus;F:Flavonoid biosynthesis;G:Flavanone biosynthesis,phenylalanine => naringenin;H:Hemicellulose metabolic process;I:Amino sugar and nucleotide sugar metabolism;J:Small molecule biosynthetic process;K:Response to toxic substance;L:Phenylpropanoid catabolic process;M:S-adenosylmethionine biosynthetic process;N:Protein folding;O:Response to water deprivation;P:Coumarin biosynthetic process;Q:Response to UV;R:Starch and sucrose metabolism;S:Cellular response to toxic substance;T:Small molecule catabolic process.

Fig. 7 Conserved motifs（Motif 1-Motif 10）of three auxin response genes in walnut

Fig. 8 Expression of three auxin related genes in walnut endocarp at sclerosis stage Different capital indicates there are significant difference in same gene at the 1% level in different periods.

Fig. 9 Expression of 12 genes related to lignin synthesis pathway “*”means that the expression of gene is significant difference between the two regions of endocarp during the same period,and“**”means that the expression of gene is extremely significant difference between the two regions of endocarp during the same period.

Fig. 10 Schematic diagram of possible‘Xinlu’walnut endocarp hardening model

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Dynamic Changes of Auxin and Analysis of Differentially Expressed Genes in Walnut Endocarp During Hardening

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