Comparative transcriptome profiling and morphology provide insights into endocarp cleaving of apricot cultivar (Prunus armeniaca L.)
- Xiao Zhang†1, 2,
- Lijie Zhang†3,
- Qiuping Zhang1, 2,
- Jiayu Xu1,
- Weisheng Liu2Email author and
- Wenxuan Dong1Email author
© The Author(s). 2017
Received: 24 August 2016
Accepted: 30 March 2017
Published: 11 April 2017
A complete and hardened endocarp is a typical trait of drupe fruits. However, the ‘Liehe’ (LE) apricot cultivar has a thin, soft, cleavable endocarp that represents 60.39% and 63.76% of the thickness and lignin content, respectively, of the ‘Jinxihong’ (JG) apricot (with normal hardened-endocarp). To understand the molecular mechanisms behind the LE apricot phenotype, comparative transcriptomes of Prunus armeniaca L. were sequenced using Illumina HiSeq™ 2500.
In this study, we identified 63,170 unigenes including 15,469 genes >1000 bp and 25,356 genes with Gene Function annotation. Pathway enrichment and expression patterns were used to characterize differentially expression genes. The DEGs encoding key enzymes involved in phenylpropanoid biosynthesis were significantly down-regulated in LE apricot. For example, CAD gene expression levels, encoding cinnamyl alcohol dehydrogenase, were only 1.3%, 0.7%, 0.2% and 2.7% in LE apricot compared with JG cultivar at 15, 21, 30, 49 days after full bloom (DAFB). Furthermore, transcription factors regulating secondary wall and lignin biosynthesis were identified. Especially for SECONDARY WALL THICKENING PROMOTING FACTOR 1 (NST 1), its expression levels in LE apricot were merely 2.8% and 9.3% compared with JG cultivar at 15 and 21 DAFB, respectively.
Our comparative transcriptome analysis was used to understand the molecular mechanisms underlie the endocarp-cleaving phenotype in LE apricot. This new apricot genomic resource and the candidate genes provide a useful reference for further investigating the lignification during development of apricot endocarp. Transcription factors such as NST1 may regulate genes involved in phenylpropanoid pathway and affect development and lignification of the endocarp.
KeywordsApricot candidate genes Comparative transcriptomes Endocarp cleaving Transcription factors
Apricot (P. armeniaca L.) is a typical drupe of the family Rosaceae with eight pairs of chromosomes (2 n = 16) . Cultivated apricots are widely cultivated around the world (Asia 59.9%, Europe 21.6%, Oceania 0.4%, Africa 15.8%, and Americas 2.3%. FAO, 2013–2014) and apricot production has a relatively high economic value. Apricot fruit has rich nutritional value, including dietary fiber, organic acids, vitamin C, carotene, and trace elements . Furthermore, the kernel is a natural plant protein resource, which used as medicine and food .
The pericarp develops from the ovary, and the innermost layer is the endocarp. The hardened endocarp has a vital role in seed protection and dispersal in some important economic fruits, such as peach, apricot, plum, almond, cherry, mango, olive, and coffee . In plant evolution, the function of the heavily lignified endocarp is to ensure secure environment for seed development [5, 6]. Endocarp hardening is a significant trait of mature drupe fruits. It is caused by the secondary wall formation and lignin deposition . Biochemical analysis has found that the endocarps of olive and peach contained much more lignin than poplar stem , suggesting that a relatively extreme degree of secondary wall formation occurs in fruit endocarp tissues. Lignin is an aromatic polymer that is widely found in the secondary walls of plants, as well as most enzymes and regulatory steps in the lignin biosynthetic pathway (phenylpropanoid pathway) have been identified . Endocarp lignification in Arabidopsis has been adequately studied in relation to dehiscence, and even the transcriptional regulatory network has also been examined . For drupe fruits, Ryugo  observed the regulation of lignin biosynthesis and accumulation in peach stones in the early 1960s. Lignification in peach endocarp is a highly coordinated process, which has been shown by subsequent developmental studies . Recently, a transcriptional network dominated by NAC and MYB genes was observed in a well-conserved regulatory pathway, which causes Arabidopsis dehiscence or peach endocarp formation , and plays an essential role in the secondary wall formation and lignification via stimulating the pathway. Furthermore, several MADs-box genes involved in the formation of fruit endocarp, including SHP1, SHP2, STK, and FUL were identified . These TFs co-function with IND, ALC , and RPL  to stimulates endocarp differentiation.
This study investigated the mechanisms of endocarp development and phenotype formation, using Illumina sequencing and expression pattern analysis of candidate genes in apricot fruits during the stages of endocarp development and lignification.
Differences in endocarp development in LE and JG apricot
The lignin deposition process was discernible from fruit transverse sections (at 24 DAFB) showing color reaction between the phloroglucinol and lignin (Fig. 3b). The lignin deposition process began at the tip of the endocarp and gradually completed over 25 days (24–49 DAFB). Interestingly, LE cultivar exhibited incomplete areas of endocarp that had little or no lignification (Fig. 3a, b). The thickness and lignin content were significantly lower in LE endocarp, which estimated by 60.4% and 63.3%, respectively; out of that in JG endocarp (Fig. 3d, e). Thus the differences in endocarp development and lignification were significant.
Illumina sequencing and assembly
Summary of RNA–seq and de novo assembly of P. armeniaca L. unigenes
Numbers of clean reads
Numbers of 200–300 bp contigs
Mean length of contigs (bp)
N50 length of contigs (bp)
Numbers of ≥200 bp transcripts
Mean length of transcripts (bp)
N50 length of transcripts (bp)
Numbers of unigenes
Mean length of unigenes (bp)
N50 length of unigenes (bp)
Length distribution of P. armeniaca L. unigenes
All combination unigenes length (bp)
Functional annotation and identification of unigenes
Summary of assembled P. armeniaca L. unigenes
Number of unigenes length ≥ 300 bp
Number of unigenes length ≥ 1000 bp
The total number of annotated unigenes
The functions of predicted genes were classified by GO analysis. A total of 16,506 genes annotated in the GO database were categorized into 57 functional groups, belonging to three main GO ontologies: biological processes, cellular components, and molecular functions (Additional file 5: Table S3; Additional file 6: Figure S3). ‘metabolic process’ (8408 genes, 50.93%), were dominant among the functional groups.
We used the KEGG pathway database to search the functional networks of biological interactions. In total, 4830 genes were identified in the KEGG database and were assigned to 118 KEGG pathways (Additional file 7: Table S4). The majority of genes was classified into pathways for ‘carbohydrate metabolism’ (905 genes), ‘translation’ (596 genes), ‘amino acid metabolism’ (581 genes), or ‘folding, sorting and degradation’ (471 genes). Biosynthesis of other secondary metabolites matched 192 genes.
Transcript differences between LE and JG apricot
Endocarp cleaving and incomplete lignin deposition in the fruit of LE apricot were highly complex phenomena that caused by a series of biological processes, including many genes acting synergistically, collaborating in regulating various pathways. However, the phenylpropanoid pathway is undoubtedly one of the most important. Endocarp hardening occurs via secondary cell wall formation and lignification. In the phenylpropanoid pathway, p-coumaryl alcohol, sinapyl alcohol, and coniferyl alcohol are the end products that form the different types of lignin monomers . From the KEGG enrichment analysis, phenylalanine metabolism, phenylpropanoid biosynthesis, and hormone signal transduction were the foremost pathways and contained the most number of DEGs in LE1_VS_JG1 (Additional file 7: Table S4; Additional file 8: Figure S4). Thirty-four DEGs associated with the phenylalanine pathway were differentially expressed.
DEGs between LE and JG apricot that involved in phenylpropanoid pathway
Fold change (log2 JG/LE)
Phenylalanine ammonia–lyase 1 [P. mume]
4–coumarate–CoA ligase [A. thaliana]
Cytochrome P450 CYP73A100 [P. ginseng]
Cytochrome P450 98A2 [P. mume]
Cytochrome P450 98A2 [P. mume]
Cinnamoyl–CoA reductase 1 [A. thaliana]
Cinnamoyl–CoA reductase 1–like [P. mume]
Caffeic acid 3–O–methyltransferase [P. mume]
Shikimate O–hydroxycinnamoyltransferase [A. thaliana]
Shikimate O–hydroxycinnamoyltransferase [A. thaliana]
Caffeoyl–CoA O–methyltransferase 1 [A. thaliana]
Cinnamyl alcohol dehydrogenase [A. thaliana]
Cinnamyl alcohol dehydrogenase [A. thaliana]
Peroxidase 72 [A. thaliana]
Peroxidase 29 [A. thaliana]
Peroxidase 12 [A. thaliana]
Peroxidase 42 [A. thaliana]
Peroxidase 4 [V. vinifera]
Peroxidase 17 [A. thaliana]
Peroxidase 51 [A. thaliana]
Aspartate aminotransferase [D. carota]
aminotransferase TAT2 [A. thaliana]
Cytochrome P450 98A3 [A. thaliana]
DEGs between LE and JG apricot that involved in secondary wall biosynthesis
Fold change (log2 JG/LE)
LE1 VS JG1
LE2 VS JG2
Agamous–like MADS–box protein AGL11 [A. thaliana]
Agamous–like MADS–box protein AGL1 [A. thaliana]
Agamous–like MADS–box protein AGL8 [A. thaliana]
BEL1–like homeodomain protein 9 [A. thaliana]
NAC domain–containing protein 43 [A. thaliana]
NAC domain–containing protein 7 [A. thaliana]
Gibberellin 3–beta–dioxygenase 1 [P. sativum]
Transcription factor MYB46 [A. thaliana]
Transcription factor MYB46 [A. thaliana]
Transcription factor MYB32 [P. mume]
The hardened endocarp has a vital role in seed protection and dispersal in some important economic fruits, such as peach, apricot, plum, almond, cherry, mango, olive, and coffee . Endocarp hardening is a significant trait of fruit matures of any types of drupes, which caused by the secondary wall formation and lignin deposition . Phenylpropanoid biosynthesis played a crucial role in endocarp lignification in both LE and JG apricot. Sequence analysis of transcriptome revealed a series of differentially expressed genes involved in the phenylpropanoid pathway, such as 4CL, HCT, COMT and CAD. Knockout of 4CL in Arabidopsis had no significant effect on either lignin content or monomeric composition . However, RNAi silencing of HCL in Arabidopsis and Radiata pine reduced lignin content and changed the monomeric composition [21, 22]. In COMT antisense Leucaena leucocephala, the lignin content was reduced to 72% by decreasing 60% of OMT activity . CAD1 made a significant contribution to the synthesis of coniferyl alcohol, and down-regulated CAD1 in wild-type tobacco has a moderate impact on G unit content of the non-condensed lignin fraction . CAD activities were drastically reduced in null mutants of Arabidopsis (AtCAD-D and AtCAD-C), and affected sinapyl alcohol dehydrogenase activity in these mutants. AtCAD-D had an significant influence on lignin content and proportion of conventional S lignin . In LE cultivar, expression of 4CL were up-regulated, yet expressions of HCL and COMT were down-regulated, which relative to JG cultivar (Figs. 6, 8). In particular, CAD expressed down-regulated in LE apricot compared with JG, in both RNA-seq data and relative gene expression (Figs. 6, 8). These results indicated that thickness and incomplete endocarp are unlikely to result from mutation of one specific phenylpropanoid pathway gene. In fact, expression levels of CAD and HCT had significant correlation with endocarp thickness and lignin content in LE apricot (Additional file 11: Table S6). These genes or TFs may be responsible for the defects in endocarp development and lignification in LE apricot.
SHP, STK and NST1 were specifically expressed in endocarp of peach. In exocarp and mesocarp, the negative regulator FUL exhibited a high expression level. However, the expression of IND and ALC was insignificant . In Arabidopsis stk shp1 shp2 triple mutants, the integuments were changed into carpel-like structures leading to complete sterility . Over-expression of FUL caused no lignin deposition in valve tissues in Arabidopsis . Furthermore, in tomato, over-expression of FUL2 lead to a thinner pericarp, and reduced stem cell layer . In a split pit resistant variety of peach, SHP expression was low, however in the sensitive variety, FUL expression was significantly elevated . Our analysis found that STK, SHP, and FUL were discovered in DEGs, but IND and ALC were not. Expression of SHP and FUL had significant different between LE and JG at 9 DAFB, while STK remained down-regulated during the S1 stage significantly. RNA-seq data and qPCR analysis reflected that SHP, STK, and FUL were highly expressed and essential for endocarp development (Table 5; Fig. 8). IND directly activates GA3ox1, which is an indispensable enzyme catalyzing the last step of GAs biosynthesis in the separation layer of Arabidopsis. IND induces GAs accumulation to degrade DELLA protein, resulting in release ALC . In atga3ox1 atga3ox2 double mutants of Arabidopsis, synthesis of cellulose, hemicelluloses, and lignin were suppressed obviously . NST1 and NST3 (SND1) have been proven as master switches that regulate the secondary wall biosynthesis and lignification in Arabidopsis , Medicago , and Poplar . In the transcriptional network, the downstream transcription factor MYBs is activated by NST1 and SND1, and multiple genes are involved in secondary wall biosynthesis . In nst1 mutants, valve margins were obvious in the absence of the secondary wall, meanwhile in nst1 nst3 double mutants, only vascular vessels conserved secondary wall formation . The SND1, and VND1–5, VND6–7 were not detected as DEGs in this study. The expression levels of VND4 were always lower in LE relative to JG cultivar at 15 and 21 days after full bloom (Additional file 3: Table S2). NST1, the domain of that regulates biosynthesis of secondary wall, lignin and xylanase always had low expression levels in LE fruit (Table 5; Fig. 8). This might be one of the main cause of cleaving and thinning of endocarp in LE apricot. Hence, NST1 was regarded as an essential candidate gene in the development and phenylpropanoid biosynthesis in endocarp of LE apricot. MYB46 is also a decisive master switch and AtMYB46 was reported to be a direct target of ANAC012/SND1/NST3 , which adjusted secondary cell wall biosynthesis . Dominant repression or over-expression of MYB46 has a considerable effect on secondary wall thickening of fibers and vessels and biosynthesis of lignin and cellulose . We identified two differentially expressed MYB46 (Table 5). In addition, MYB46 could activate the expression of MYB4, MYB7, and MYB32 , and the MYB32 protein sequence was highly similar to that of MYB4 . AtMYB4 regulates the expression of C4H, so that AtMYB32 could negatively regulate several genes implicated in phenylpropanoid biosynthesis . Trans-activation assays and transgenic studies also show that MYB32 appears to be a negative regulator of SND1 expression . Interestingly, MYB32 was extraordinary up-regulated in LE, and expression of C4H down-regulated (Fig. 8) only in LE fruit. MYB32 of apricot might also play an important part in negative regulating the lignin biosynthesis in the secondary wall.
Common expression pattern analysis provided a new understanding of the expression and function of DEGs, and combines pathways with multiple candidate genes, which were related to the flavonoid pathway and cell function (Fig. 7; Additional file 9: Table S5). CHS1 and F3H expressed higher level in LE than JG, which may cause by considerable down-expression of CAD. However, DFR had a down-regulated expression. Among 408 genes in Cluster 1, CSLG3, and related genes, CSLA9  and KATAM had significant higher level expression in LE during stage S1 and S2 relative to JG cultivar. Furthermore, ARR5 and ARR16 regulators appeared to act as negative regulators of Cytokinin signaling , and showed significantly up-regulated expression in LE apricot.
Our results implied that cleaving of endocarp in LE apricot started at 15 DAFB, and this area increased during fruit development. The thickness and lignin content of the mature LE endocarp was only 60.39% and 63.25%, respectively, compared with JG endocarp (Fig. 3). RNA-Seq to sequencing and de novo assembly of the fruit transcriptomes of two cultivars of P. armeniaca (L.) showed discrepancies in development and lignification of the endocarp and explained the cleaving of endocarp in LE apricot. The DEGs and qPCR analysis data (Fig. 8) identified differentially expression genes involved in TFs (STK, SHP, FUL, NST1, MYB46, MYB32) and phenylpropanoid, flavonoid and hormone pathways (4CL, HCT, COMT, CAD, CHS1, F3H, DFR, GA3ox1, ARR5, and ARR16), consistent with endocarp phenotype and lignin content. Our results indicated that TFs especially NST1, may regulate genes of the phenylpropanoid pathway. Besides, low expression level of NST1 may inhibit the endocarp development and lignification of LE apricot.
‘Liehe’ (LE) apricot, synonym as ‘Luoren’ apricot, and ‘Jinxihong’ (JG) apricot are local cultivars originated respectively in Linyuan City and Jinxi County of Liaoning Province and were collected into National Germplasm Repository (N40°10′1.18″, E122°09′39.41″) for Plums and Apricots at Xiongyue, Liaoning, China in 1983. LE and JG, with the accession number XC0347 and XC0015 based on the Chinese National Key Project “Exploration, Collection, Conservation of Plum and Apricot Germplasm Resources” funded by the Agricultural Ministry of China. The identification of LE and JG cultivar was done by the Liaoning Institute of Pomology [43, 44]. During the 2015 season, the fruits of LE and JG were picked in National Germplasm Repository for Plums and Apricots from 6 DAFB (50% of flowers had opened) including all the developmental stages of fruit, with the permission of the curator, Dr. Weisheng LIU, of National Germplasm Repository for Plums and Apricots and used in this study. The seeds were separated from the fruit which were picked. The stages were characterized by weight and shape (horizontal and vertical diameter). Fruits were sliced, frozen in liquid N2, and stored at −80 °C for RNA extraction.
Measurement of fruit growth and endocarp lignification
Fresh fruit diameter were measured (horizontal and vertical diameter) by digital Vernier caliper (0–150 mm ± 0.02 mm), and weighted using electronic scales (300 g/0.01 g). The fitting for each equation were used the Pearl-Reed logistic [45, 46] and normal logistic equation  as references. The first derivative of equation was calculated and drew by MATLAB 8.5 (Math Works, US). The expression levels of transcripts encoding ACO1 and PEPCK were analysis used the same method . Flower buds, flowers and young fruits were observed using an Olympus SZX7 microscope to examine the cleaving of the endocarp. Developing endocarp areas were calculated using Olympus cellSens software. Fruit samples for lignin deposition observation were collected once every 3 days from 15 to 43 DAFB. Observation and lignin content tests were conducted using Alba’s method . The measurements for each index were repeated three times in 10 samples. Means and analysis of variance (ANOVA) were separated using Duncan’s Multiple Range Test (DMRT) in SPSS 19.0 (IBM, US).
cDNA library preparation and Illumina sequencing
Total RNAs were extracted from fruit samples without kernels using Gambino’s method . The RNA samples were examined with an Agilent 2100 Bioanalyzer (US). cDNA library preparation and sequencing of fruits at 15 DAFB (LE1, JG1) and 21 DAFB (LE2, JG2) with two replicates per each cultivar, were conducted by the Biomarker Technology Company (Beijing, China). The cDNA library used high-throughput sequencing (RNA-seq) with the Illumina HiSeq™ 2500. Reads length of sequences was PE125.
Sequence assembly and functional annotation
A large number of raw reads was produced using Sequencing by Synthesis (SBS) from Illumina HiSeq™ 2500. The Trinity method  was used for de novo assembly of Illumina reads of the two apricot cultivars. Clean reads were mapped to the genome of Prunus mume and Prunus persica using TopHat Software . Genes were first aligned using BLASTx (E value <105) to the NCBI non-redundant protein databases (NR) . The alignments from the NR database were used blast2GO (https://www.blast2go.com/) to get GO annotation . The number of DEGs which matched to three categories was counted, and GO ontology figure was drawn by Graph-R Project. The statistical method of GO enrichment was “right sided Fisher exact test”. The term was Core ontology (go.obo, http://purl.obolibrary.org/obo/go.obo). The main parameter of BLASTx is “blastx -task blastx-fast -num_descriptions 100 -num_alignments 100 -evalue 1e-5”. This parameter was used to blast databases. The annotation of genes were performed using the method were as follows: Swiss-Port protein databases , COG , KOG  KEGG . Predicted amino acid sequences were aligned by hidden Markov models (HMMER, E value <1010)  to the Protein family (Pfam)  to annotate the genes. Coding sequence (CDS) of genes were predicted by TransDecoder Software (http://transdecoder.github.io).
Differentially expression genes analysis
Gene expression levels were analyzed using fragments per kilobase of the transcript per million mapped reads (FPKM) method . DESeq Software  was used to identify DEGs in pair-wise comparisons, and the results of all statistical tests were revised to account for multiple testing with the Benjamini–Hochberg false discovery rate (FDR <0.01). Sequences were determined to be significantly differentially expressed at a P value (<0.01), and Fold change (FC) >2. Common expression pattern analysis using BMKCloud (https://www.biocloud.net/) was applied twice to serial samples. Euclidean distance was used in the Distance method and K-means for hierarchical clustering. Hierarchical clustering was conducted using Spotfire DecisionSite 8.1 (Spotfire Inc., http://spotfire.tibco.com/).
Quantitative RT-PCR analysis
A total of 500 ng of RNAs was used to synthesize cDNA using PrimeScript™RT Kit (Cat. RR047A, TaKaRa, Japan). The cDNA was diluted five times, and then used as a template. The reaction solution contained SYBR® PremixExTaq™ II (Tli RNaseH Plus) (Cat. RR820A, TaKaRa, Japan) and was conducted in an ABI 7500 Real Time PCR Detection System (Applied Biosystems, US). Quantitative primers for validation of DEGs are listed in Additional file 12: Table S7. The relative expression levels of the selected genes, normalized to peach ACT  and P. mume ACT7 (unigene, c48143.c0), were calculated using the 2-ΔCt method. All reactions were performed with three biological replicates. Three technical replicates were in each biological replicate. The analysis of variance (ANOVA) was based on Duncan’s Multiple Range Test (DMRT) in SPSS 19.0 (IBM, US).
1-aminocyclopropane-1-carboxylic acid oxidase 1
Basic helix-loop-helix genes ALCATRAZ
Two-component response regulator ARR16
Two-component response regulator ARR5
Cinnamyl alcohol dehydrogenase
Chalcone synthase 1
Clusters of orthologous groups databases
Cellulose synthase 3
Days after full bloom
Differentially expression genes
Duncan’s Multiple Range Test
Fragments per kilobase of the transcript per million mapped reads
MADS-Box genes FRUITFUL
Gibberellin 3-beta-dioxygenase 1
Gene ontology databases
Basic helix-loop-helix genes INDEHISCENT
Xyloglucan galactosyltransferase KATAMARI1 homolog
Kyoto encyclopedia of genes and genomes pathway databases
euKaryotic orthologous groups databases
NCBI non-redundant protein databases
SECONDARY WALL THICKENING PROMOTING FACTOR
Quantitative real-time PCR
- REPLUMLESS :
BEL1-like homeodomain gene
MADS-box genes SHATTERPROOF
MADS-box genes SEEDSTIC
Protein VASCULAR RELATED NAC-DOMAIN 1–7
Xyloglucan endotransglucosylase/hydrolase 2
We thank Dr. Hamad, Dr. Zhang Qijing and Dr. Hou Yali for assisting with the experiments and commenting on the manuscript.
This work was supported by: the Program of Conservation and Utilization of Crop Germplasm Resources-Apricot and Plum (2014–2016); National Natural Science Foundation of China (31401826); Hawthorn Program of National Crop Germplasm Resources Infrastructure (2014–2016).
Availability of data and materials
The data supporting the results presented in this article are included as additional files.
The RNA-seq data has been deposited in Sequence Read Archives Database (https://www.ncbi.nlm.nih.gov/sra/) under accession number SRP083125.
Conceived and designed the experiments: ZX, LWS, and DWX Performed the experiments: ZX, ZQP, and ZLJ. Analyzed the data: ZX, ZLJ, XJY and DWX. Wrote the paper: ZX, LWS, and DWX. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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