Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (4): 759-778.doi: 10.3864/j.issn.0578-1752.2025.04.011

• HORTICULTURE • Previous Articles     Next Articles

Dynamics of Fruit Hollowness and Browning and Associated Lignin Accumulation and Its Genome-Wide Identification of Ps4CL Gene Family in Huangguan Plum

LI JianKun(), PENG Chao, ZHANG ZiYang, LIANG Xi, WEI MingKang, YANG Qiang, LI BinQi, Muhammad Moaaz Ali, Viola Kayima, CHEN FaXing(), DENG HongHong()   

  1. College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002
  • Received:2024-06-28 Accepted:2024-09-04 Online:2025-02-16 Published:2025-02-24
  • Contact: CHEN FaXing, DENG HongHong

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Abstract:

【Objective】The objective of this study was to examine the temporal dynamics of hollowness and browning (HB) in Nai plum during its fruit development and ripening, to evaluate the relationship between HB and lignin accumulation, and to identify the 4CL gene family in Huangguan plum, a critical gene in the lignin biosynthetic pathway, at the whole-genome level. 【Method】Huangguan plum fruits were sampled at 10, 25, 40, 55, 70, and 80 days after full bloom to investigate the dynamics of HB. Anatomical changes in fruit structure induced by HB were observed by using paraffin sectioning. Lignin monomers were identified by using gas chromatography-mass spectrometry (GC-MS), while lignin content and associated enzyme activities were measured via UV-spectrophotometer. Gene expression was quantitatively analyzed through quantitative reverse transcription polymerase chain reaction (qRT-PCR). The genome-wide identification of the 4CL gene family was conducted utilizing tools, such as NCBI, TBtools, MEME, MEGA11, SOPMA, SWISS-MODEL, and PlantCARE. 【Result】HB initiated at the veraison stage, with the HB rate reaching 37.73% at the mature stage. Additionally, the fruit shape index of HB plum was significantly higher than that of non-HB plum. Histological analysis using paraffin section showed that the HB pulp was stained red by Saffron-O and Fast Green Stain and the HB area increased as the fruit developed. The total lignin content exhibited a gradual increase during fruit development and ripening, with the total lignin content in HB fruit being significantly higher than that in non-HB fruit (P≤0.001). The lignin monomers in HB fruit were predominantly composed of guaiacyl lignin (22.6%) and syringly lignin (10.8%). Both 4CL and PAL enzyme activities were significantly elevated in HB fruit compared with non-HB fruit during fruit development and ripening period. Expression levels of eight Ps4CLs were higher in HB fruit compared to non-HB fruit, with similar trends observed for two PsPALs which showed slightly higher expression in HB fruit during veraison stage. Ps4CL1, Ps4CL2, Ps4CL7, and Ps4CL8 were potentially implicated in the biosynthesis of lignin of plum fruit. The Ps4CL gene family characterized by a significant number of cis-acting elements associated with plant endogenous hormones. Collinearity analysis indicated the presence of two and eight pairs of 4CL homologous genes between plum and the Arabidopsis and peach, respectively. Weighted gene co-expression network analysis (WGCNA) identified core hub genes (Ps4CL5, Ps4CL7, and Ps4CL8), each exhibiting co-expression with at least 30 other genes. The qRT-PCR results demonstrated that Ps4CL genes exhibit tissue-specific and temporally specific expression profiles. 【Conclusion】This paper identified the critical period for HB occurrence (the veraison stage) and characterized the dynamics of lignin content, monomer type, enzyme activity, and related gene expression in Huangguan plum. WGNCA highlighted key genes involved in the lignin biosynthetic pathway in Huangguan plum, which laid a foundation for further exploration of regulatory mechanisms, control strategies, and related molecular mechanisms of HB in plum fruit.

Key words: plum, fruit hollowness and browning, lignin biosynthesis, enzyme activity, 4CL gene family

Table 1

Real-time fluorescence quantitative primers of 4CL and PAL genes"

基因Gene 上游引物Forward primer (5'→3') 下游引物Reverse primer (5'→3')
CAC GGGATACGCTACAAGAAGAATGAG CTTACACTCTGGCATACCACTCAA
Ps4CL1 ATTTGTGGGTTGTGCCTCCT TGGCACAGTCCTCCATCAAC
Ps4CL2 GCGACTCTGCTCTACTCGTC AGGAACCTCTCCTCCCCATC
Ps4CL3 CAGCTCCATTCCCGACCTTT ACGGAGCGAATTGGGGATTT
Ps4CL4 TGATAGGCCCGGAAGAGTCA AGGAGGTAAGGCCTCTCTGG
Ps4CL5 CATCGCTTTCGCCACATCAG TTTGGTTGACCTCGACTCCG
Ps4CL6 GCCATCGCTTTCGTCACATC GATCCGACCCGATTGAGCAT
Ps4CL7 AACTCAGTCGGACACTGCTG GCGAGCCCATAGATGTGGAA
Ps4CL8 CCAACTCCATCCACTTCCCC GGTGATGACGAGTTTGGGGT
PsPAL1 TGCAAGGGCTGCATTGGATA GGTACTCTGCACCCAACTCC
PsPAL2 TTTGGTTGCACTTTGCCAGG GCTCCCCAGTCACTCCAAAA
PsPAL3 CACACATTGCCTCACACAGC GCCAATCAAAAGCCCAGCAA

Fig. 1

Phenotype of Huangguan plum fruit without (A) and with (B) hollowness and browning"

Fig. 2

Single fruit weight (A), fruit shape index (B), correlation relationship between cavity horizontal diameter and fruit vertical diameter (C), correlation relationship between cavity vertical diameter and fruit vertical diameter (D), soluble solids content (E), and malic acid content (F) of Huangguan plum fruit with and without hollowness and browning"

Fig. 3

Paraffin sections of Huangguan plum fruit with and without hollowness and browning"

Fig. 4

Ultraviolet spectroscopic scanning profile (A), total lignin content (B), GC-MS total ion flow pattern of derivatization followed by reductive cleavage (DFRC) products (C), mass spectrum of DFRC products (D), lignin monomer type and content (E) of Huangguan plum flesh"

Fig. 5

The enzyme activity of 4CL (A) and PAL (B) of Huangguan plum fruit with and without hollowness and browning"

Fig. 6

The gene expression of 4CL in Huangguan plum fruit with and without hollowness and browning"

Fig. 7

The gene expression of PsPAL1 (A) and PsPAL2 (B) in Huangguan plum fruit with and without hollowness and browning"

Table 2

Basic information of Ps4CL gene family members in plum"

基因
Gene		 基因编号
Gene id		 长度
Lengh (aa)		 分子量
Mw (kDa)		 等电点
pI		 不稳定系数
Instability index (II)		 脂肪系数
Aliphatic index		 平均亲水性
GRAVY		 亚细胞定位
Subcellular localization
Ps4CL1 PsSY0000530.1 542 59125.61 8.63 35.93 99.57 -0.009 过氧化物酶体Peroxisome
Ps4CL2 PsSY0028946.1 567 61306.62 8.84 40.42 99.75 -0.013 过氧化物酶体Peroxisome
Ps4CL3 PsSY0000072.1 562 60031.21 8.02 36.90 102.14 -0.017 过氧化物酶体Peroxisome
Ps4CL4 PsSY0002508.1 557 61097.49 6.49 33.24 96.12 -0.033 过氧化物酶体Peroxisome
Ps4CL5 PsSY0008604.1 558 60955.14 6.26 37.26 98.69 0.077 过氧化物酶体Peroxisome
Ps4CL6 PsSY0008690.1 558 60987.40 6.11 33.51 97.16 0.019 过氧化物酶体Peroxisome
Ps4CL7 PsSY0029187.1 542 58714.25 5.85 42.44 97.76 0.115 过氧化物酶体Peroxisome
Ps4CL8 PsSY0029483.1 544 59775.10 8.63 52.05 97.7 0.012 过氧化物酶体Peroxisome

Fig. 8

Phylogenetic tree of 4CL gene family in plum, Arabidopsis thaliana, and apple"

Fig. 9

Localization of 4CL gene family in plum"

Fig. 10

The conservative motif (A) and gene family structure (B) of 4CL gene family in plum"

Fig. 11

The tertiary structural model of the Ps4CL protein in plum"

Fig. 12

Promoter cis-acting elements (A) and collinearity analysis (B) of the Ps4CL in plum"

Fig. 13

The cluster dendrogram of module characteristic genes (A), hierarchical clustering dendrogram of co-expression modules (B), correlation heap map of co-expression modules with different developmental periods (C), and potential co-expression gene of the core hub Ps4CL genes (D) of the weighted correlation network analysis of the transcriptome data of Huangguan plum The letters F, G, V, and M in A and C represent developmental stages of Huangguan plum, i.e., fruitlet, green expansion, veraison, and maturation stages, respectively"

Fig. 14

Expression analysis of 4CL gene family in different tissues and fruit development stages of Huangguan plum The 10, 25, 40, 55, 70, and 85 in x-axis represent different stages of Huangguan plum fruit development, which are expressed as 10, 25, 40, 55, 70, and 85 days after flowering, respectively. The letters NC and C represent the non-cavity and cavity fruit samples, respectively"

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