Genome-wide identification of PEBP gene family members in potato, their phylogenetic relationships, and expression patterns under heat stress.
Abiotic stress response
Expression patterns
High temperature stress
PEBP gene family analysis
PEBP motifs
Phylogenetic relationships
Solanum tuberosum L.
Tandem and segmental duplications
Journal
Molecular biology reports
ISSN: 1573-4978
Titre abrégé: Mol Biol Rep
Pays: Netherlands
ID NLM: 0403234
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
12
08
2021
accepted:
02
03
2022
pubmed:
4
4
2022
medline:
14
7
2022
entrez:
3
4
2022
Statut:
ppublish
Résumé
The phosphatidylethanolamine-binding protein (PEBP) gene family is involved in regulating many plant traits. Genome-wide identification of PEPB members and knowledge of their responses to heat stress may assist genetic improvement of potato (Solanum tuberosum). We identified PEBP gene family members from both the recently-updated, long-reads-based reference genome (DM v6.1) and the previous short-reads-based annotation (PGSC DM v3.4) of the potato reference genome and characterized their heat-induced gene expression using RT-PCR and RNA-Seq. Fifteen PEBP family genes were identified from DM v6.1 and named as StPEBP1 to StPEBP15 based on their locations on 6 chromosomes and were classified into FT, TFL, MFT, and PEBP-like subfamilies. Most of the StPEBP genes were found to have conserved motifs 1 to 5. Tandem or segmental duplications were found between StPEBP genes in seven pairs. Heat stress induced opposite expression patterns of certain FT and TFL members but involving different members in leaves, roots and tubers. The long-reads-based genome assembly and annotation provides a better genomic resource for identification of PEBP family genes. Heat stress tends to decrease FT gene activities but increases TFL gene activities, but this opposite expression involves different FT/TFL pairs in leaves, roots, and tubers. This tissue-specific expression pattern of PEBP members may partly explain why different potato organs differ in their sensitivities to heat stress. Our study provides candidate PEBP family genes and relevant information for genetic improvement of heat tolerance in potato and may help understand heat-induced responses in other plants.
Sections du résumé
BACKGROUND
BACKGROUND
The phosphatidylethanolamine-binding protein (PEBP) gene family is involved in regulating many plant traits. Genome-wide identification of PEPB members and knowledge of their responses to heat stress may assist genetic improvement of potato (Solanum tuberosum).
METHODS AND RESULTS
RESULTS
We identified PEBP gene family members from both the recently-updated, long-reads-based reference genome (DM v6.1) and the previous short-reads-based annotation (PGSC DM v3.4) of the potato reference genome and characterized their heat-induced gene expression using RT-PCR and RNA-Seq. Fifteen PEBP family genes were identified from DM v6.1 and named as StPEBP1 to StPEBP15 based on their locations on 6 chromosomes and were classified into FT, TFL, MFT, and PEBP-like subfamilies. Most of the StPEBP genes were found to have conserved motifs 1 to 5. Tandem or segmental duplications were found between StPEBP genes in seven pairs. Heat stress induced opposite expression patterns of certain FT and TFL members but involving different members in leaves, roots and tubers.
CONCLUSION
CONCLUSIONS
The long-reads-based genome assembly and annotation provides a better genomic resource for identification of PEBP family genes. Heat stress tends to decrease FT gene activities but increases TFL gene activities, but this opposite expression involves different FT/TFL pairs in leaves, roots, and tubers. This tissue-specific expression pattern of PEBP members may partly explain why different potato organs differ in their sensitivities to heat stress. Our study provides candidate PEBP family genes and relevant information for genetic improvement of heat tolerance in potato and may help understand heat-induced responses in other plants.
Identifiants
pubmed: 35366758
doi: 10.1007/s11033-022-07318-z
pii: 10.1007/s11033-022-07318-z
doi:
Substances chimiques
Plant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4683-4697Subventions
Organisme : National Natural Science Foundation of China
ID : 31860399
Organisme : Agriculture and Agri-Food Canada
ID : A-base research funding
Organisme : Natural Sciences and Engineering Research Council of Canada
ID : RGPIN 2017-04589
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Tang R, Niu S, Zhang G, Chen G, Haroon M, Yang Q, Rajora OP, Li X-Q (2018) Physiological and growth responses of potato cultivars to heat stress. Botany 96:897–912. https://doi.org/10.1139/cjb-2018-0125
doi: 10.1139/cjb-2018-0125
Zhang G, Tang R, Niu S, Si H, Yang Q, Bizimungu B, Regan S, Li X-Q (2020) Effects of earliness on heat stress tolerance in fifty potato cultivars. Am J Potato Res 97:23–32. https://doi.org/10.1007/s12230-019-09740-9
doi: 10.1007/s12230-019-09740-9
Karlgren A, Gyllenstrand N, Källman T, Sundström JF, Moore D, Lascoux M, Lagercrantz U (2011) Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution. Plant Physiol 156:1967–1977. https://doi.org/10.1104/pp.111.176206
Panjama K, Suzuki E, Otani M, Nakano M, Ohtake N, Ohyama T, Bundithya W, Sueyoshi K, Ruamrungsri S (2019) Isolation and functional analysis of FLOWERING LOCUS T orthologous gene from Vanda hybrid. J Plant Biochem Biotechnol 28:374–381. https://doi.org/10.1007/s13562-019-00487-2
doi: 10.1007/s13562-019-00487-2
Yu X, Liu H, Sang N, Li Y, Zhang T, Sun J, Huang X (2019) Identification of cotton MOTHER OF FT AND TFL1 homologs, GhMFT1 and GhMFT2, involved in seed germination. PLoS ONE 14:e0215771. https://doi.org/10.1371/journal.pone.0215771
Nose M, Kurita M, Tamura M, Matsushita M, Hiraoka Y, Iki T, Hanaoka S, Mishima K, Tsubomura M, Watanabe A (2020) Effects of day length- And temperature-regulated genes on annual transcriptome dynamics in Japanese cedar (Cryptomeria japonica D. Don), a gymnosperm indeterminate species. PLoS ONE. https://doi.org/10.1371/journal.pone.0229843
doi: 10.1371/journal.pone.0229843
pubmed: 32150571
pmcid: 7062269
Hedman H, Källman T, Lagercrantz U (2009) Early evolution of the MFT-like gene family in plants. Plant Mol Biol 70:359–369. https://doi.org/10.1007/s11103-009-9478-x
Adeyemo OS, Hyde PT, Setter TL (2019) Identification of FT family genes that respond to photoperiod, temperature and genotype in relation to flowering in cassava (Manihot esculenta, Crantz). Plant Reprod 32:181–191. https://doi.org/10.1007/s00497-018-00354-5
Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962. https://doi.org/10.1126/science.286.5446.1960
Danilevskaya ON, Meng X, Hou Z, Ananiev EV, Simmons CR (2008) A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol 146:250–264. https://doi.org/10.1104/pp.107.109538
Chardon F, Damerval C (2005) Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol 61:579–590. https://doi.org/10.1007/s00239-004-0179-4
Abelenda JA, Navarro C, Prat S (2014) Flowering and tuberization: a tale of two nightshades. Trends Plant Sci 19:115–122. https://doi.org/10.1016/j.tplants.2013.09.010
Borovsky Y, Mohan V, Shabtai S, Paran I (2020) CaFT-LIKE is a flowering promoter in pepper and functions as florigen in tomato. Plant Sci. https://doi.org/10.1016/j.plantsci.2020.110678
doi: 10.1016/j.plantsci.2020.110678
pubmed: 33218641
Dong L, Lu Y, Liu S (2020) Genome-wide member identification, phylogeny and expression analysis of PEBP gene family in wheat and its progenitors. PeerJ 8:e10483. https://doi.org/10.7717/peerj.10483
Nakano Y, Higuchi Y, Sumitomo K, Oda A, Hisamatsu T, Naro (2015) Delay of flowering by high temperature in chrysanthemum: heat-sensitive time-of-day and heat effects on CsFTL3 and CsAFT gene expression. J Hortic Sci Biotechnol 90:143–149. https://doi.org/10.1080/14620316.2015.11513165
Gaire R, Wilde HD (2018) Natural allelic variation in blueberry TERMINAL FLOWER 1. Plant Genetic Resour 16:59–67. https://doi.org/10.1017/S1479262116000435
doi: 10.1017/S1479262116000435
Zhang X, Wang C, Pang C, Wei H, Wang H, Song M, Fan S, Yu S (2016) Characterization and functional analysis of PEBP family genes in upland cotton (Gossypium hirsutum L.). PLoS ONE 11:e0161080. https://doi.org/10.1371/journal.pone.0161080
Navarro C, Abelenda JA, Cruz-Oró E, Cuéllar CA, Tamaki S, Silva J, Shimamoto K, Prat S (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478:119–123. https://doi.org/10.1038/nature10431
doi: 10.1038/nature10431
pubmed: 21947007
Morris WL, Alamar MC, Lopez-Cobollo RM, Castillo Cañete J, Bennett M, Van der Kaay J, Stevens J, Kumar Sharma S, McLean K, Thompson AJ (2019) A member of the TERMINAL FLOWER 1/CENTRORADIALIS gene family controls sprout growth in potato tubers. J Exp Bot 70:835–843. https://doi.org/10.1093/jxb/ery387
Zhang X, Campbell R, Ducreux LJ, Morris J, Hedley PE, Mellado-Ortega E, Roberts AG, Stephens J, Bryan GJ, Torrance L, Chapman SN, Prat S, Taylor MA (2020) TERMINAL FLOWER-1/CENTRORADIALIS inhibits tuberisation via protein interaction with the tuberigen activation complex. Plant J 103:2263–2278. https://doi.org/10.1111/tpj.14898
Hancock RD, Morris WL, Ducreux LJ, Morris JA, Usman M, Verrall SR, Fuller J, Simpson CG, Zhang R, Hedley PE (2014) Physiological, biochemical and molecular responses of the potato (Solanum tuberosum L.) plant to moderately elevated temperature. Plant Cell Environ 37:439–450. https://doi.org/10.1111/pce.12168
Sequencing TPG (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189. https://doi.org/10.1038/nature10158
Pham GM, Hamilton JP, Wood JC, Burke JT, Zhao H, Vaillancourt B, Ou S, Jiang J, Buell CR (2020) Construction of a chromosome-scale long-read reference genome assembly for potato. GigaScience 9: 1–11. https://doi.org/10.1093/gigascience/giaa100
Eddy SR (2004) What is a hidden Markov model? Nat Biotechnol 22:1315–1316. https://doi.org/10.1038/nbt1004-1315
Wang M, Tan Y, Cai C, Zhang B (2019) Identification and expression analysis of phosphatidy ethanolamine-binding protein (PEBP) gene family in cotton. Genomics 111(6):1373–1380. https://doi.org/10.1016/j.ygeno.2018.09.009
Letunic I, Khedkar S, Bork P (2021) SMART: recent updates, new developments and status in 2020. Nucl Acids Res 49:D458–D460. https://doi.org/10.1093/nar/gkaa937
Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, De Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E (2012) ExPASy: SIB bioinformatics resource portal. Nucl Acids Res 40:W597–W603. https://doi.org/10.1093/nar/gks400
Consortium U (2015) UniProt: a hub for protein information. Nucl Acids Res 43:D204–D212. https://doi.org/10.1093/nar/gky1131
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucl Acids Res 47:D607–D613. https://doi.org/10.1093/nar/gky1131
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucl Acids Res 39:W316–W322. https://doi.org/10.1093/nar/gkr483
doi: 10.1093/nar/gkr483
pubmed: 21715386
pmcid: 3125809
Kotoda N, Hayashi H, Suzuki M, Igarashi M, Hatsuyama Y, Kidou S-i, Igasaki T, Nishiguchi M, Yano K, Shimizu T (2010) Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus× domestica Borkh.). Plant Cell Physiol 51:561–575. https://doi.org/10.1093/pcp/pcq021
Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (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
doi: 10.1093/nar/gkr1293
pubmed: 22217600
pmcid: 3326336
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
doi: 10.1093/molbev/msw054
pubmed: 27004904
pmcid: 8210823
Wang D, Zhang Y, Zhang Z, Zhu J, Yu J (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genom Proteom Bioinf 8:77–80. https://doi.org/10.1016/s1672-0229(10)60008-3
doi: 10.1016/s1672-0229(10)60008-3
Liu Z, Coulter JA, Li Y, Zhang X, Meng J, Zhang J, Liu Y (2020) Genome-wide identification and analysis of the Q-type C2H2 gene family in potato (Solanum tuberosum L.). Int J Biol Macromol 153:327–340. https://doi.org/10.1016/j.ijbiomac.2020.03.022
doi: 10.1016/j.ijbiomac.2020.03.022
pubmed: 32145229
Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 280:187–198. https://doi.org/10.1007/s00438-008-0355-0
doi: 10.1007/s00438-008-0355-0
pubmed: 18563445
Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B, Cui X, Peng L (2010) Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol 10:282. https://doi.org/10.1186/1471-2229-10-282
doi: 10.1186/1471-2229-10-282
pubmed: 21167079
pmcid: 3022907
Lu K, Li T, He J, Chang W, Zhang R, Liu M, Yu M, Fan Y, Ma J, Sun W (2017) qPrimerDB: a thermodynamics-based gene-specific qPCR primer database for 147 organisms. Nucl Acids Res 46:D1229–D1236. https://doi.org/10.1093/nar/gkx725
Tang R, Gupta SK, Niu S, Li X-Q, Yang Q, Chen G, Zhu W, Haroon M (2020) Transcriptome analysis of heat stress response genes in potato leaves. Mol Biol Rep 47:4311–4321. https://doi.org/10.1007/s11033-020-05485-5
doi: 10.1007/s11033-020-05485-5
pubmed: 32488578
Xiang H, Li X-Q (2016) Development of TBSPG pipelines for refining unique mapping and repetitive sequence detection using the two halves of each Illumina sequence read. Plant Mol Biol Rep 34:172–181. https://doi.org/10.1007/s11105-015-0912-8
doi: 10.1007/s11105-015-0912-8
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106–R117. https://doi.org/10.1186/gb-2010-11-10-r106
Zhang G, Tang R, Niu S, Si H, Yang Q, Rajora OP, Li X-Q (2021) Heat-stress-induced sprouting and differential gene expression in growing potato tubers: comparative transcriptomics with that induced by postharvest sprouting. Hortic Res 8:226. https://doi.org/10.1038/s41438-021-00680-2
Sattelmacher B, Marschner H, Kühne R (1990) Effects of root zone temperature on root activity of two potato (Solanum tuberosum L.) clones with different adaptation to high temperature. J Agro Crop Sci 165:131–137. https://doi.org/10.1111/j.1439-037X.1990.tb00843.x
Sattelmacher B, Marschner H, Kühne R (1990) Effects of the temperature of the rooting zone on the growth and development of roots of potato (Solanum tuberosum). Ann Bot 65:27–36. https://doi.org/10.1093/oxfordjournals.aob.a087974
Moraes TS, Dornelas MC, Martinelli AP (2019) FT/TFL1: calibrating plant architecture. Front Plant Sci 10:97. https://doi.org/10.3389/fpls.2019.00097
Lehretz GG, Sonnewald S, Hornyik C, Corral JM, Sonnewald U (2019) Post-transcriptional regulation of FLOWERING LOCUS T modulates heat-dependent source-sink development in potato. Curr Biol 29:1614-1624.e3. https://doi.org/10.1016/j.cub.2019.04.027
doi: 10.1016/j.cub.2019.04.027
pubmed: 31056391
Hastilestari BR, Lorenz J, Reid S, Hofmann J, Pscheidt D, Sonnewald U, Sonnewald S (2018) Deciphering source and sink responses of potato plants (Solanum tuberosum L.) to elevated temperatures. Plant Cell Environ 41:2600–2616. https://doi.org/10.1111/pce.13366