Abstract
Vacuolar processing enzymes (VPEs) play important roles in plant development, programmed cell death, and the responsiveness to biotic and abiotic stresses. To characterize the VPEs in upland cotton (Gossypium hirsutum), the VPE gene family within four Gossypium species, consisting of G. hirsutum, G. barbadense, G. arboreum, and G. raimondii, together with Arabidopsis thaliana, was comparatively analyzed at the genome-wide level. As a result, a total of 43 VPEs were identified, including 13 GhVPEs, 12 GbVPEs, 7 GaVPEs, and 7 GrVPEs, which are evenly distributed with one gene on a chromosome from four Gossypium species, respectively. The phylogenetic tree showed that the identified VPEs within the four Gossypium species could be categorized into β-type, δ-type, and γ-type VPE clades. Collinearity analysis presented 36 of intraspecies VPE-pairs and 152 of interspecies VPE-pairs, respectively, which are included in synteny blocks on chromosome. These results indicate that VPE duplication events have accorded well with the whole genome duplication. And expression profiles of GhVPEs in G. hirsutum seedlings demonstrated that the GhVPEs from the same clade are not necessarily identical in the pattern of transcriptional expression. Upon abiotic stresses (i.e., waterlogging and salt treatments), three GhVPEs (i.e., Ghir_A05G004610, Ghir_A09G011870, and Ghir_D09G011410) were significantly upregulated in their expression amounts, respectively. The GhVPE genes that presented inducible expression under some abiotic stresses may be applied to the improvement of resilience to abiotic stresses for the cultivated cottons.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Genome data of A. thaliana, G. raimondii, and G. arboreum, on the database Phytozome (https://phytozome.jgi.doe.gov). Genome data of G. hirsutum and G. barbadense, on the Gossypium new sequence database (http://ibi.zju.edu.cn/cotton). Information of the identified VPEs in Table 1, included in the manuscript.
References
Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141. https://doi.org/10.1016/j.pbi.2005.01.001
Albertini A, Simeoni F, Galbiati M, Bauer H, Tonelli C, Cominelli E (2014) Involvement of the vacuolar processing enzyme γVPE in response of Arabidopsis thaliana to water stress. Biol Plantarum 58:531–538. https://doi.org/10.1007/s10535-014-0417-6
Ariizumi T, Higuchi K, Arakaki S, Sano T, Asamizu E, Ezura H (2011) Genetic suppression analysis in novel vacuolar processing enzymes reveals their roles in controlling sugar accumulation in tomato fruits. J Exp Bot 62:2773–2786. https://doi.org/10.1093/jxb/erq451
Bundy MGR, Kosentka PZ, Willet AH, Zhang L, Miller E, Shpak ED (2016) A mutation in the catalytic subunit of the glycosylphosphatidylinositol transamidase disrupts growth, fertility, and stomata formation. Plant Physiol 171:974–985. https://doi.org/10.1104/pp.16.00339
Cheng ZY, Guo XR, Zhang JX, Liu YD, Wang B, Li H, Lu H (2020) βVPE is involved in tapetal degradation and pollen development by activating proprotease maturation in Arabidopsis thaliana. J Exp Bot 71:1943–1955. https://doi.org/10.1093/jxb/erz560
Cheng ZY, Zhang JX, Yin B, Liu YD, Wang B, Li H, Lu H (2019) γVPE plays an important role in programmed cell death for xylem fiber cells by activating protease CEP1 maturation in Arabidopsis thaliana. Int J Biol Macromol 137:703–711. https://doi.org/10.1016/j.ijbiomac.2019.07.017
Chen ZW, Cao JF, Zhang XF, Shangguan XX, Mao YB, Wang LJ, Chen XY (2017) Cotton genome: challenge into the polyploidy. Sci Bull 62:1622–1623. https://doi.org/10.1016/j.scib.2017.11.022
Christoff AP, Turchetto-Zolet AC, Margis R (2014) Uncovering legumain genes in rice. Plant Sci 215–216:100–109. https://doi.org/10.1016/j.plantsci.2013.11.005
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Gong PJ, Yan L, Tang YJ, Rong W, Zhu HJ, Wang YJ, Zhang CH (2018) Vacuolar processing enzyme (VvβVPE) from Vitis vinifera, processes seed proteins during ovule development, and accelerates seed germination in VvβVPE heterologously over-expressed Arabidopsis. Plant Sci 274:420–431. https://doi.org/10.1016/j.plantsci.2018.06.023
Guan B, Lin Z, Liu D, Li C, Zhou Z, Mei F, Li J, Deng X (2019) Effect of waterlogging-induced autophagy on programmed cell death in Arabidopsis roots. Front Plant Sci 10:468. https://doi.org/10.3389/fpls.2019.00468
Han JJ, Lin W, Oda Y, Cui KM, Fukuda H, He XQ (2012) The proteasome is responsible for caspase-3-like activity during xylem development. Plant J 72:129–141. https://doi.org/10.1111/j.1365-313X.2012.05070.x
Hara-Nishimura I, Hatsugai N, Nakaune S, Kuroyanagi M, Nishimura M (2005) Vacuolar processing enzyme: an executor of plant cell death. Curr Opin Plant Biol 8:404–408. https://doi.org/10.1016/j.pbi.2005.05.016
Hara-Nishimura I, Inoue K, Nishimura M (1991) A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms. FEBS Lett 294:89–93. https://doi.org/10.1016/0014-5793(91)81349-D
Hara-Nishimura I, Kinoshita T, Hiraiwa N, Nishimura M (1998) Vacuolar processing enzymes in protein-storage vacuoles and lytic vacuoles. J Plant Physiol 152:668–674. https://doi.org/10.1016/S0176-1617(98)80028-X
Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 5685:855–858. https://doi.org/10.1126/science.1099859
Hatsugai N, Yamada K, Goto-Yamada S, Hara-Nishimura I (2015) Vacuolar processing enzyme in plant programmed cell death. Front Plant Sci 6:234. https://doi.org/10.3389/fpls.2015.00234
Hu Y, Chen JD, Fang L, Zhang ZY, Ma W, Niu YC, Ju LZ, Deng JQ, Zhao T et al (2019) Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nat Genet 51:739–748. https://doi.org/10.1038/s41588-019-0371-5
Julián I, Gandullo J, Santos-Silva LK, Diaz I, Martinez M (2013) Phylogenetically distant barley legumains have a role in both seed and vegetative tissues. J Exp Bot 64:2929–2941. https://doi.org/10.1093/jxb/ert132
Kinoshita T, Nishimura M, Hara-Nishimura I (1995) The sequence and expression of the γ-VPE gene, one member of a family of three genes for vacuolar processing enzymes in Arabidopsis thaliana. Plant Cell Physiol 36:1555–1562. https://doi.org/10.1093/oxfordjournals.pcp.a078921
Kinoshita T, Yamada K, Hiraiwa N, Kondo M, Nishimura M, Hara-Nishimura I (1999) Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions. Plant J 19:43–53. https://doi.org/10.1046/j.1365-313X.1999.00497.x
Kuroyanagi M, Nishimura M, Hara-Nishimura I (2002) Activation of Arabidopsis vacuolar processing enzyme by self-catalytic removal of an auto-inhibitory domain of the C-terminal propeptide. Plant Cell Physiol 43:143–151. https://doi.org/10.1093/pcp/pcf035
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Li DH, Wu D, Li SZ, Dai Y, Cao YP (2019) Evolutionary and functional analysis of the plant-specific NADPH oxidase gene family in Brassica rapa L. Roy Soc Open Sci 6:181727. https://doi.org/10.1098/rsos.181727
Li FG, Fan GY, Lu CR, Xiao GH, Zou CS, Kohel RJ, Ma ZY, Shang HH et al (2015) Genome sequence of cultivated upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol 33:524–530. https://doi.org/10.1038/nbt.3208
Nakaune S, Yamada K, Kondo M, Kato T, Tabata S, Nishimura M, Hara-Nishimura I (2005) A vacuolar processing enzyme, δVPE, is involved in seed coat formation at the early stage of seed development. Plant Cell 17:876–887. https://doi.org/10.1105/tpc.104.026872
Poncet V, Scutt C, Tournebize R, Villegente M, Cueff G, Rajjou L, Balliau T, Zivy M, Fogliani B, Job C, de Kochko A, Sarramegna-Burtet V, Job D (2015) The Amborella vacuolar processing enzyme family. Front Plant Sci 6:618. https://doi.org/10.3389/fpls.2015.00618
Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. https://doi.org/10.1371/journal.pone.0009490
Radchuk V, Weier D, Radchuk R, Weschke W, Weber H (2010) Development of maternal seed tissue in barley is mediated by regulated cell expansion and cell disintegration and coordinated with endosperm growth. J Exp Bot 62:1217–1227. https://doi.org/10.1093/jxb/erq348
Rojo E, Martín R, Carter C, Zouhar J, Pan S, Plotnikova J, Jin H, Paneque M, Sánchez-Serrano JJ, Baker B, Ausubel FM, Raikhel NV (2004) VPEgamma exhibits a caspase-like activity that contributes to defense against pathogens. Curr Biol 14:1897–1906. https://doi.org/10.1016/j.cub.2004.09.056
Shimada T, Yamada K, Kataoka M, Nakaune S, Koumoto Y, Kuroyanagi M, Tabata S, Kato T, Shinozaki K, Seki M, Kobayashi M, Kondo M, Nishimura M, Hara-Nishimura I (2003) Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J Biol Chem 278:32292–32299. https://doi.org/10.1074/jbc.M305740200
Song JF, Yang F, Xun M, Xu LX, Tian XZ, Zhang WW, Yang HQ (2020) Genome-wide identification and characterization of vacuolar processing enzyme gene family and diverse expression under stress in apple (Malus × domestic). Front Plant Sci 11:626. https://doi.org/10.3389/fpls.2020.00626
Tang YJ, Wang RP, Gong PJ, Li SX, Wang YJ, Zhang CH (2016) Gene cloning, expression and enzyme activity of Vitis vinifera vacuolar processing enzymes (VvVPEs). PLoS ONE 11:e0160945. https://doi.org/10.1371/journal.pone.0160945
Teper-Bamnolker P, Buskila Y, Lopesco Y, Ben-Dor S, Saad I, Holdengreber V, Belausov E, Zemach H, Ori N, Lers A, Eshel D (2012) Release of apical dominance in potato tuber is accompanied by programmed cell death in the apical bud meristem. Plant Physiol 158:2053–2067. https://doi.org/10.1104/pp.112.194076
Vorster BJ, Cullis CA, Kunert KJ (2019) Plant vacuolar processing enzymes. Front Plant Sci 10:479. https://doi.org/10.3389/fpls.2019.00479
Wagner A (2002) Selection and gene duplication: a view from the genome. Genome Biol 3:reviews1012.1–1012.3. https://doi.org/10.1186/gb-2002-3-5-reviews1012
Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49. https://doi.org/10.1093/nar/gkr1293
Yamada K, Basak AK, Goto-Yamada S, Tarnawska-Glatt K, Hara-Nishimura I (2020) Vacuolar processing enzymes in the plant life cycle. New Phytol 226:21–31. https://doi.org/10.1111/nph.16306
Zakharov A, Müntz K (2004) Seed legumains are expressed in stamens and vegetative legumains in seeds of Nicotiana tabacum L. J Exp Bot 55:1593–1595. https://doi.org/10.1093/jxb/erh166
Zhang HP, Tao X, Zhang F (2021) Genome-wide identification and expression analysis of the vacuolar processing enzyme (VPE) family genes in pear. J Hortic Sci Biotech 96:469–478. https://doi.org/10.1080/14620316.2021.1882887
Funding
This research was funded by the Natural Science Foundation of Anhui Province, China (1808085MC58); the State Key Laboratory of Cotton Biology Open Fund, China (CB2018A13); and the Innovation Practice Project of Undergraduate Students of Anhui Province, China (201910364178).
Author information
Authors and Affiliations
Contributions
DL designed the investigation. LZ and XW performed the data analysis and experiment. JT and XZ performed the data analysis. TY and YL performed the experiment. DL wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
10142_2021_818_MOESM2_ESM.xlsx
Supplementary file2 Primer pairs for detecting the transcriptional expression of GhVPEs using qRT-PCR method (XLSX 24 KB)
Supplementary Fig. 1
(PNG 46993 KB)
10142_2021_818_MOESM4_ESM.tiff
High Resolution Image Sequence logos of the conserved domains of Peptidase_C13. The alignment was performed based on the amino-acid sequences of Peptidase_C13 from 43 VPEs identified. Histidine (H) and cystine (C), the essential residues for catalytic activity, are marked by boxes (TIFF 8015 KB)
Supplementary Fig. 2
(PNG 6129 KB)
10142_2021_818_MOESM5_ESM.tiff
High Resolution Image Phylogenetic tree constructed based on the amino-acid sequences of 41 VPEs, without two VPEs (Ghir_A06G009480 and Gorai.011G060200) containing incomplete sequences of Peptidase_C13. Three subgroups are indicated with I–III, among which subgroups I, II and III are categorized as β-type, δ-type, and γ-type VPEs, respectively. The Arabidopsis AtGPI8 (AT1G08750) and its potential homolog (Ghir_A11G027160) in G. hirsutum, were used as outgroup (OG). Asterisks mark the VPE IDs. Bootstrap-support was represented by circle at the individual node (TIFF 881 KB)
Supplementary Fig. 3
(PNG 17550 KB)
10142_2021_818_MOESM6_ESM.tiff
High Resolution Image Collinearity relationships between GbVPEs and GaVPEs (a), GrVPEs (b), GaVPEs and GrVPEs (c), or between AtVPEs and GbVPEs (d), GaVPEs (e), and GrVPEs (f), respectively. Chromosomes of Arabidopsis, G. barbadense, G. arboreum, and G. raimondii, are indicated with T1–T5, a1–d13, CA1–CA13, and CR1–CR13, respectively. Orange linkages indicate the intraspecies synteny blocks, while green ones refer to the interspecies synteny blocks, which contain the VPE gene-pairs with collinearity. The gene IDs labeled on chromosomes are VPEs identified (TIFF 2510 KB)
Rights and permissions
About this article
Cite this article
Zhu, L., Wang, X., Tian, J. et al. Genome-wide analysis of VPE family in four Gossypium species and transcriptional expression of VPEs in the upland cotton seedlings under abiotic stresses. Funct Integr Genomics 22, 179–192 (2022). https://doi.org/10.1007/s10142-021-00818-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-021-00818-4