Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (18): 3728-3743.doi: 10.3864/j.issn.0578-1752.2025.18.011

• HORTICULTURE • Previous Articles     Next Articles

Genome-Wide Identification and Expression Analysis of Peroxiredoxins Gene Family in Asparagus officinalis

YI ZeHui(), WANG Ying, SONG HuiXia, ZHAO Jing, MAO LiPing   

  1. College of Horticulture, Shanxi Agricultural University/Shanxi Key Laboratory of Germplasm Resources Innovation and Utilization of Vegetable and Flower, Taiyuan 030031
  • Received:2025-04-25 Accepted:2025-06-19 Online:2025-09-18 Published:2025-09-18

Abstract:

【Objective】The peroxiredoxin (Prx) gene family in garden asparagus was systematically identified at the genome-wide level. The tissue-specific expression profiles and responses to abiotic stress, dormancy, and dormancy release were comprehensively investigated, providing a critical foundation for further functional characterization and breeding applications of AoPrxs. 【Method】Using the genomic data of asparagus, the members of the Prx family were identified through bioinformatics methods. The physicochemical properties, subcellular localization, gene structures, and conserved motifs of the AoPrxs were predicted using ProtParam, Cell-PLoc 2.0, SWISS-MODEL, and MEME tools, respectively. The tissue-specific expression patterns of AoPrxs and their responses to diverse stresses, dormancy, and dormancy release were systematically analyzed using RNA-Seq data and real-time fluorescent quantitative PCR (qRT-PCR). 【Result】The AoPrx family contains six members, designated AoPrx1-AoPrx6, all of which contain the conserved PXXXTXXC sequence. Their amino acid sequences ranged from 162 to 268 residues, with molecular weights ranging from 17 397.96 to 29 246.45 Da. A total of 220 (38 types) cis-acting elements were identified in AoPrxs, including those involved in plant growth and development, stress response, hormone signaling, and light response. Collinearity analysis revealed that AoPrx has a higher homology with TaPrx and OsPrx. Phylogenetic analysis classified the AoPrxs into five subfamilies, each exhibiting highly conserved gene structures, amino acid sequences, and protein structures. Notably, AoPrx1 and AoPrx2 lack the ‘resolving’ Cys residue but exhibit greater similarity in both amino acid sequence and protein structure to members of the PrxⅡB subfamily than to those of the 1-Cys subfamily. Consequently, they were classified into the PrxⅠB subfamily. Tissue expression analysis showed that AoPrx2 is ubiquitously expressed across all tissues, in contrast to AoPrx5, which showed stamen-specific upregulation in supermale flowers. The expression profile under adverse stress conditions indicated that salt-alkali stress significantly upregulated AoPrx5 expression in the roots of asparagus seedlings. Additionally, salt, drought, and low-light treatments markedly enhanced AoPrx4 expression levels in the stems and leaves of asparagus seedlings, while infection by Phomopsis asparagi exerted an opposite regulatory effect on AoPrx4 expression. Furthermore, AoPrx2, AoPrx4, and AoPrx5 may also be involved in the regulatory processes of dormancy induction and release in asparagus. 【Conclusion】Six Prx family members were identified in the asparagus genome, distributed across five chromosomes. All members contained the conserved PXXXTXXC motif and were phylogenetically classified into five subfamilies. Expression profiling revealed subfunctionalization among Prx paralogs: AoPrx5 was closely associated with stamen development and root salt tolerance. AoPrx4 played a pivotal role in the responses of stem and leaf tissues to salt, drought, low-light conditions, and phomopsis asparagi stress. Moreover, AoPrx2, AoPrx4, and AoPrx5 were also involved in the regulation of asparagus dormancy induction and release.

Key words: Asparagus officinalis L., Prx gene family, genome-wide identification, bioinformatics, expression analysis

Table 1

Primers used for qRT-PCR"

基因Gene 基因ID Gene ID 正向引物Forward primer (5′-3′) 反向引物Reverse primer (5′-3′)
AoUBI LOC109836288 ACACCATCGGCGATCTCAAG TTGACATCTTTGACAACCTTGTGG
AoPrx1 LOG109848397 GCTCCCCATGCATTCCCTT TAGGTTTTTGCCCATGCCTTC
AoPrx2 LOG109848405 AGCATGTGCCGAGTTTCATC GCGTGAGTGTAGGTTCCAGAT
AoPrx3 LOG109830907 ACGATTGCTTGCGTCTCAGT CGCTCTCGTAAAGTCCCCAT
AoPrx4 LOG109836803 CTTGCTTCAAACCCGAAGGC GCTCAATCCGCTGAAGCTCT
AoPrx5 LOG109842952 ATGACGTGGAGAGCCACAAG CTGACCCTTGTCATCGTGCT
AoPrx6 LOG109822385 ATCCTGCTGATGAGACCCCT CCCCGCTTATTCCTACCACC

Fig. 1

Multiple sequence alignment of Prx protein in garden asparagus"

Table 2

Analysis of physicochemical properties of Prx genes in garden asparagus"

基因
Gene
基因ID
GeneID
CDS长度
CDS length (bp)
氨基酸数
Amino acid number
分子量
Molecular weight (Da)
等电点
pI
不稳定系数
Instability index
亲水性GRAVY 亚细胞定位
Subcellular localization
AoPrx1 LOC109848397 489 162 17397.96 4.99 30.46 0.017 细胞质、细胞核Cytoplasm, nucleus
AoPrx2 LOC109848405 489 162 17455.09 5.54 36.71 0.015 细胞质Cytoplasm
AoPrx3 LOC109830907 534 177 18906.72 5.27 33.81 0.001 细胞核Nucleus
AoPrx4 LOC109836803 807 268 29246.45 6.18 39.63 -0.051 叶绿体、细胞质Chloroplast, cytoplasm
AoPrx5 LOC109842952 657 218 24097.49 5.28 34.82 -0.375 细胞核Nucleus
AoPrx6 LOC109822385 645 214 23642.20 9.53 51.42 -0.416 叶绿体、细胞核Chloroplast, nucleus

Fig. 2

Classification of the plant Prx protein family and the conservation of each subfamily"

Fig. 3

Phylogenetic tree of PrxⅡB protein sequences genes in garden asparagus, Arabidopsis, Upland cotton, rice and wheat Ao: Asparagus officinalis; At: Arabidopsis thaliana; Gh: Gossypium hirsutum; Os: Oryza sativa; Ta: Triticum aestivum"

Fig. 4

Phylogenetic tree of Prx protein of garden asparagus, Arabidopsis, Upland cotton, rice and wheat A: Amino acid sequence; B: Putative three-dimensional structure"

Fig. 5

Phylogenetic tree and gene structure of Prx gene family in garden asparagus A: Phylogentic tree of AoPrx protein; B: AoPrx conserved motif; C: AoPrx gene structure; D: Domain location; E: Sequence logos of some conserved motifs"

Fig. 6

Characteristics of secondary structure of Prx proteins in garden asparagus"

Fig. 7

Predicted tertiary structures of Prx proteins in garden asparagus"

Fig. 8

Putative Cis-acting existed in the 2 000 bp upstream region of AoPrx gene family"

Fig. 9

Chromosome location of AoPrx gene family"

Fig. 10

Colinear analysis of Prx gene family in garden asparagus, Arabidopsis, Upland cotton, wheat and rice"

Fig. 11

Tissue expression analysis of Prx gene family in garden asparagus"

Fig. 12

The response of Prx gene family in garden asparagus to stresses (A), dormancy and releasing dormancy (B) S1: Salt stress Ⅰ, S-0h, S-6h, and S-48h indicates the salt stress time was 0, 6, and 48 hours, respectively; S2: Salt stress Ⅱ, FD and GJ refer to the varieties Fengdao and Champion, while S and PI denote salt stress and inoculation with Piriformospora indica; S3: Salt stress Ⅲ, P0, P1, and P2 indicates the NaCl concentrations was 0, 171 and 342 mmol·L-1, respectively; D1: Drought stress, J and P represent the varieties Jinglv No. 3 and Pacific Early, with DS signifying drought stress; L1: Weak-light stress, Light-25. Light-45, Light-65, and Light-100% refers to light intensity was 25%, 45%, 65%, and 100% of normal light, respectively; PI1: Phomopsis asparagi stress, PI-0h. PI-24h and PI-48h denotes the sampling time was 0, 24 and 48 hours post-inoculation, respectively; A1 and A2 refer to the dormancy and dormancy release. F20 and S20 represent the fall and spring of 2020, GM and UC stand for the varieties Guelph Millennium and UC157, A-C indicate the 1st to 3rd sampling, and Rz, Bu, and BL refer to rhizome, dormant bud, and growing bud, respectively. The same as below"

Fig. 13

The qRT-PCR analysis of AoPrx in different tissues (A) and under salt stress conditions (B) M: Male; F: Female"

[1]
陈光宇. 中国芦笋产业发展现状与趋势. 世界农业, 2013(10): 181-186, 188.
CHEN G Y. The status quo and trends for the development of Asparagus industry in China. World Agriculture, 2013(10): 181-186, 188. (in Chinese)
[2]
SACHDEV S, ANSARI S A, ANSARI M I, FUJITA M, HASANUZZAMAN M. Abiotic stress and reactive oxygen species: Generation, signaling, and defense mechanisms. Antioxidants, 2021, 10(2): 277.
[3]
RHEE S G. Overview on peroxiredoxin. Molecules and Cells, 2016, 39(1): 1-5.

doi: 10.14348/molcells.2016.2368 pmid: 26831451
[4]
孙豪, 孙晨. 过氧化物还原酶(peroxiredoxin)家族研究进展. 生命的化学, 2023, 43(10): 1569-1578.
SUN H, SUN C. Research progress of peroxiredoxin family. Chemistry of Life, 2023, 43(10): 1569-1578. (in Chinese)
[5]
BERNROITNER M, ZAMOCKY M, FURTMÜLLER P G, PESCHEK G A, OBINGER C. Occurrence, phylogeny, structure, and function of catalases and peroxidases in cyanobacteria. Journal of Experimental Botany, 2009, 60(2): 423-440.

doi: 10.1093/jxb/ern309 pmid: 19129167
[6]
BOURGONJE A R, VAN GOOR H, BAKKER S J L, HILLEBRANDS J L, BILO H J G, DULLAART R P F, VAN DIJK P R. Serum peroxiredoxin-4, a biomarker of oxidative stress, is associated with the development of nephropathy in patients with type 2 diabetes (Zodiac-65). Free Radical Biology and Medicine, 2024, 212: 186-190.

doi: 10.1016/j.freeradbiomed.2023.12.025 pmid: 38151214
[7]
左溪如, 王淘, 陈烨, 闫亚娜, 黄桂艳, 李瑞民. 柑橘黄龙病菌过氧化物还原酶基因CLasPrx的克隆及功能分析. 植物保护学报, 2024, 51(3): 654-662.
ZUO X R, WANG T, CHEN Y, YAN Y N, HUANG G Y, LI R M. Cloning and functional analysis of a peroxiredoxin gene, CLasPrx, from huanglongbing pathogen Candidatus Liberibacter asiaticus. Journal of Plant Protection, 2024, 51(3): 654-662. (in Chinese)
[8]
AIHAITI Y, TUERHONG X, ZHENG H S, CAI Y S, YANG M Y, XU P. Peroxiredoxin 4 regulates tumor-cell-like characteristics of fibroblast-like synoviocytes in rheumatoid arthritis through PI3k/Akt signaling pathway. Clinical Immunology, 2022, 237: 108964.
[9]
GAO D D, LV Y, HONG F, WU D, WANG T, GAO G, LIN Z J, YANG R Y, HU J S, HE A L, ZHANG P Y. Peroxiredoxin 6 maintains mitochondrial homeostasis and promotes tumor progression through ROS/JNK/p38 MAPK signaling pathway in multiple myeloma. Scientific Reports, 2025, 15: 70.
[10]
RAN X Q, GAO L, YAN M, KANG C J. Peroxiredoxin 4 interacts with domeless and participates in antibacterial immune response through the JAK/STAT pathway. Frontiers in Immunology, 2022, 13: 907183.
[11]
ZHOU F L, CHEN F, OUYANG Z W, ZHU R D, ZHOU R P, HU W, LU C. Functions of peroxiredoxins and their roles in autoimmune diseases. Antioxidants & Redox Signaling, 2024, 40(4/5/6): 329-344.
[12]
KIM Y, JANG H H. The role of peroxiredoxin family in cancer signaling. Journal of Cancer Prevention, 2019, 24(2): 65-71.

doi: 10.15430/JCP.2019.24.2.65 pmid: 31360686
[13]
WU M Y, DENG C J, LO T H, CHAN K Y, LI X, WONG C M. Peroxiredoxin, senescence, and cancer. Cells, 2022, 11(11): 1772.
[14]
MISHRA D, SHEKHAR S, CHAKRABORTY S, CHAKRABORTY N. Wheat 2-Cys peroxiredoxin plays a dual role in chlorophyll biosynthesis and adaptation to high temperature. The Plant Journal, 2021, 105(5): 1374-1389.

doi: 10.1111/tpj.15119 pmid: 33283912
[15]
WANG Y Y, LIU Z Y, WANG P L, JIANG B, LEI X J, WU J, DONG W F, GAO C Q. A 2-Cys peroxiredoxin gene from Tamarix hispida improved salt stress tolerance in plants. BMC Plant Biology, 2020, 20: 360.
[16]
XIAO G L, ZHAO M M, LIU Q H, ZHOU J Z, CHENG Z H, WANG Q N, XIA G M, WANG M C. TaBAS1 encoding a typical 2-Cys peroxiredoxin enhances salt tolerance in wheat. Frontiers in Plant Science, 2023, 14: 1152375.
[17]
WANG J C, SONG J Q, QI H L, ZHANG H J, WANG L, ZHANG H B, CUI C C, JI G X, MUHAMMAD S, SUN G Y, XU Z R, ZHANG H H. Overexpression of 2-Cys Peroxiredoxin alleviates the NaHCO3 stress-induced photoinhibition and reactive oxygen species damage of tobacco. Plant Physiology and Biochemistry, 2023, 201: 107876.
[18]
XU A Q, CHENG F, ZHOU S, HU H, BIE Z L. Chilling-induced H2O2 signaling activates the antioxidant enzymes in alleviating the photooxidative damage caused by loss of function of 2-Cys peroxiredoxin in watermelon. Plant Stress, 2022, 6: 100108.
[19]
HERNÁNDEZ M L, JIMÉNEZ-LÓPEZ J, CEJUDO F J, PÉREZ-RUIZ J M. 2-Cys peroxiredoxins contribute to thylakoid lipid unsaturation by affecting ω-3 fatty acid desaturase 8. Plant Physiology, 2024, 195: 1521-1535.

doi: 10.1093/plphys/kiae102 pmid: 38386701
[20]
UMATE P. Genome-wide analysis of thioredoxin fold superfamily peroxiredoxins in Arabidopsis and rice. Plant Signaling & Behavior, 2010, 5(12): 1543-1546.
[21]
FENG Y L, WEI R H, LIU A Y, FAN S M, CHE J C, ZHANG Z, TIAN B M, YUAN Y L, SHI G Y, SHANG H H. Genome-wide identification, evolution, expression, and alternative splicing profiles of peroxiredoxin genes in cotton. PeerJ, 2021, 9: e10685.
[22]
LI Y H, ZHANG L M, XU J J, ZHU J X, WANG L, CHEN C J, XU H Y, ZHENG Y, LI C H, MU Z S, et al. Basic leucine zipper (bZIP) family in asparagus (Asparagus officinalis): Genome-wide identification, evolutionary, structure, collinearity, and expression analyses under abiotic stress at the seeding stage. Journal of Plant Interactions, 2023, 18(1): 2268627.
[23]
LI S F, ZHANG G J, ZHANG X J, YUAN J H, DENG C L, GAO W J. Comparative transcriptome analysis reveals differentially expressed genes associated with sex expression in garden asparagus (Asparagus officinalis). BMC Plant Biology, 2017, 17: 143.
[24]
IDE M, MASUDA K, TSUGAMA D, FUJINO K. Death of female flower microsporocytes progresses independently of meiosis-like process and can be accelerated by specific transcripts in Asparagus officinalis. Scientific Reports, 2019, 9: 2703.
[25]
WEN S S, YING J L, YE Y J, CAI Y F, QIAN R J. Comprehensive transcriptome analysis of Asparagus officinalis in response to varying levels of salt stress. BMC Plant Biology, 2024, 24: 819.
[26]
ZHANG X H, HAN C Z, WANG Y B, LIU T, LIANG Y Q, CAO Y P. Integrated analysis of transcriptomics and metabolomics of garden asparagus (Asparagus officinalis L.) under drought stress. BMC Plant Biology, 2024, 24(1): 563.
[27]
ABDELRAHMAN M, NAKABAYASHI R, MORI T, IKEUCHI T, MORI M, MURAKAMI K, OZAKI Y, MATSUMOTO M, URAGAMI A, TSUJIMOTO H, TRAN L P, KANNO A. Comparative metabolome and transcriptome analyses of susceptible Asparagus officinalis and resistant wild A. kiusianus reveal insights into stem blight disease resistance. Plant & Cell Physiology, 2020, 61(8): 1464-1476.
[28]
MA J Y, LI X Y, HE M L, LI Y W, LU W, LI M Y, SUN B, ZHENG Y X. A joint transcriptomic and metabolomic analysis reveals the regulation of shading on lignin biosynthesis in asparagus. International Journal of Molecular Sciences, 2023, 24(2): 1539.
[29]
GILL A S, WOLYN D J. Transcriptomic analysis of Asparagus officinalis cultivars with varying levels of freezing tolerance over fall acclimation and spring deacclimation periods. Frontiers in Plant Science, 2024, 15: 1442784.
[30]
陈尘, 韩立敏, 化文平, 杨晓潼. 丹参DHAR家族基因的鉴定及表达模式分析. 园艺学报, 2020, 47(11): 2181-2193.
CHEN C, HAN L M, HUA W P, YANG X T. Identification and expression analysis of dehydroascorbate reductase (DHAR) gene family in Salvia miltiorrhiza. Acta Horticulturae Sinica, 2020, 47(11): 2181-2193. (in Chinese)
[31]
于婷婷, 李欢, 宁源生, 宋建飞, 彭璐琳, 贾竣淇, 张玮玮, 杨洪强. 苹果GRAS全基因组鉴定及其对生长素的响应分析. 园艺学报, 2023, 50(2): 397-409.

doi: 10.16420/j.issn.0513-353x.2021-1039
YU T T, LI H, NING Y S, SONG J F, PENG L L, JIA J Q, ZHANG W W, YANG H Q. Genome-wide identification of GRAS gene family in apple and expression analysis of its response to auxin. Acta Horticulturae Sinica, 2023, 50(2): 397-409. (in Chinese)

doi: 10.16420/j.issn.0513-353x.2021-1039
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