Identification of Two Enzymes for Trehalose Synthesis and Their Potential Function in Growth and Development in Peanut (Arachis hypogaea)

Genome Analysis of the Encoding Trehalose Synthesis Enzymes in Peanut




Gene identification, trehalose-6-phosphate synthase, trehalose-6-phosphate phosphatase, peanut (Arachis hypogaea)


Plant trehalose has been regarded to play a key role in various biological processes during the growth and development stages. Trehalose-6-phosphate synthase (TPS) and trehalose-6-phosphate phosphatase (TPP) are two important enzymes for the synthesis of plant trehalose. Up till now, the TPS and TPP gene families have been identified and characterized in numerous higher plant species, but are rarely recorded in peanuts (Arachis hypogaea). In this study, a comprehensive search was performed to identify all putative TPS and TPP proteins in the peanut genome using Arabidopsis TPS and TPP proteins as queries. We then analyzed the characteristics of TPS and TPP members, including physic-chemical parameters, subcellular localization, phylogeny relationships, gene duplication, and expression patterns by various computational tools. As a result, a total of 17 ArahyTPS and 15 ArahyTPP genes were identified and annotated in the peanut genome, which was expanded by segmental duplication events. Our Neighbor-Joining based phylogenetic tree indicated that the ArahyTPS and ArahyTPP proteins could be categorized into three and two major branches. Gene structures and protein features analysis exhibited that the ArahyTPS and ArahyTPP proteins shared high structural and functional similarities. Based on previous RNA-Seq datasets, a majority of the ArahyTPS and ArahyTPP genes were found to specifically express in at least one major organ/tissue during the growth and development. This work will not only lead to a solid foundation on reveal the potential roles of ArahyTPS and ArahyTPP gene families in peanuts but also provide evidence to related trehalose research in other higher plant species.


Wadood SA, Nie J, Li C et al. (2022) Geographical origin classification of peanuts and processed fractions using stable isotopes. Food chemistry: X 16:100456. doi: 10.1016/j.fochx.2022.100456.

Toomer OT (2018) Nutritional chemistry of the peanut (Arachis hypogaea). Critical Reviews in Food Science and Nutrition 58 (17): 3042-3053. doi: 10.1080/10408398.2017.1339015.

Hill GM (2002) Peanut by-products fed to cattle. The veterinary clinics of North America Food animal practice 18 (2): 295-315. doi: 10.1016/s0749-0720(02)00019-1.

Dong Q, Zhao X, Zhou D et al. (2022) Maize and peanut intercropping improves the nitrogen accumulation and yield per plant of maize by promoting the secretion of flavonoids and abundance of Bradyrhizobium in rhizosphere. Frontiers in Plant Science 13: 957336. doi: 10.3389/fpls.2022.957336.

Alae-Carew C, Nicoleau S, Bird FA et al. (2020) The impact of environmental changes on the yield and nutritional quality of fruits, nuts and seeds: a systematic review. Environmental Research Letters 15 (2): 023002. doi: 10.1088/1748-9326/ab5cc0.

Iordachescu M, Imai R (2008) Trehalose biosynthesis in response to abiotic stresses. Journal of Integrative Plant Biology 50 (10):1223-9. doi: 10.1111/j.1744-7909.2008.00736.x.

Paul MJ, Gonzalez-Uriarte A (2018) The role of Trehalose 6-phosphate in crop yield and resilience. Plant Physiology 177(1):12-23. doi: 10.1104/pp.17.01634.

Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G (2006) Insights on the evolution of trehalose biosynthesis. BMC Ecology and Evolution 6:109. doi: 10.1186/1471-2148-6-109.

Grennan AK (2007) The role of trehalose biosynthesis in plants. Plant Physiology 144 (1):3-5. doi: 10.1104/pp.104.900223.

Ponnu J, Wahl V, Schmid M (2011) Trehalose-6-phosphate: connecting plant metabolism and development. Frontiers in Plant Science 2: 70. doi: 10.3389/fpls.2011.00070.

Vandesteene L, López-Galvis L, Vanneste K et al. (2012) Expansive evolution of the trehalose-6-phosphate phosphatase gene family in Arabidopsis. Plant Physiology 160 (2): 884-896. doi: 10.1104/pp.112.201400.

Rahman MM, Rahman MM, Eom J-S, Jeon J-S (2021) Genome-wide Identification, Expression Profiling and Promoter Analysis of Trehalose-6-Phosphate Phosphatase Gene Family in Rice. Journal of Plant Biology 64 (1): 55-71. doi: 10.1007/s12374-020-09279-x.

Zang B, Li H, Li W et al. (2011) Analysis of trehalose-6-phosphate synthase (TPS) gene family suggests the formation of TPS complexes in rice. Plant Molecular Biology 76 (6):507-22. doi: 10.1007/s11103-011-9781-1.

Acosta-Pérez P, Camacho-Zamora BD, Espinoza-Sánchez EA et al. (2020) Characterization of Trehalose-6-phosphate synthase and Trehalose-6-phosphate phosphatase genes and analysis of its differential xxpression in maize (Zea mays) seedlings under drought stress. Plants (Basel) 9 (3). doi: 10.3390/plants9030315.

Gao Y, Yang X, Yang X et al. (2021) Characterization and expression pattern of the trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase gene families in Populus. International Journal of Biological Macromolecules 187: 9-23. doi: 10.1016/j.ijbiomac.2021.07.096.

Song J, Mao H, Cheng J et al. (2021) Identification of the trehalose-6-phosphate synthase gene family in Medicago truncatula and expression analysis under abiotic stresses.

Gene 787:145641. doi: 10.1016/j.gene.2021.145641.

Hu M, Xie M, Cui X et al. (2022) Genome-wide characterization of Trehalose-6-phosphate synthase gene family of Brassica napus and potential links with agronomic traits. International Journal of Molecular Sciences 23 (24): 15714. doi: 10.3390/ijms232415714.

Du L, Li S, Ding L et al. (2022) Genome-wide analysis of trehalose-6-phosphate phosphatases (TPP) gene family in wheat indicates their roles in plant development and stress response. BMC Plant Biology 22 (1): 120. doi: 10.1186/s12870-022-03504-0.

Wang W, Cui H, Xiao X et al. (2022) Genome-wide identification of cotton (Gossypium spp.) Trehalose-6-phosphate phosphatase (TPP) gene family members and the role of GhTPP22 in the response to drought stress. Plants 11 (8). doi: 10.3390/plants11081079.

Liu K, Zhou Y (2022) Genome-wide identification of the trehalose-6-phosphate synthase gene family in sweet orange (Citrus sinensis) and expression analysis in response to phytohormones and abiotic stresses. PeerJ 10:e13934. doi: 10.7717/peerj.13934.

Mollavali M, Börnke F (2022) Characterization of Trehalose-6-phosphate synthase and Trehalose-6-phosphate phosphatase genes of tomato (Solanum lycopersicum L.) and analysis of their differential expression in response to temperature. International Journal of Molecular Sciences 23 (19): 11436. doi: 10.3390/ijms231911436.

Zhuang W, Chen H, Yang M et al. (2019) The genome of cultivated peanut provides insight into legume karyotypes, polyploid evolution and crop domestication. Nature Genetics 51 (5): 865-876. doi: 10.1038/s41588-019-0402-2.

Goodstein DM, Shu S, Howson R et al. (2012) Phytozome: A comparative platform for green plant genomics. Nucleic Acids Research 40 (Database issue): D1178-D86. doi: 10.1093/nar/gkr944.

Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. In Baxevanis AD et al., eds. Current protocols in bioinformatics. Chapter 2: Unit 2.3. doi: 10.1002/0471250953.bi0203s00.

Mistry J, Chuguransky S, Williams L et al. (2021) Pfam: The protein families database in 2021. Nucleic Acids Research 49 (D1): D412-D9. doi: 10.1093/nar/gkaa913.

Gasteiger E, Gattiker A, Hoogland C et al. (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research 31 (13): 3784-8. doi: 10.1093/nar/gkg563.

La HV, Chu HD, Tran CD et al. (2022) Insights into the gene and protein structures of the CaSWEET family members in chickpea (Cicer arietinum), and their gene expression patterns in different organs under various stress and abscisic acid treatments. Gene 819: 146210. doi: 10.1016/j.gene.2022.146210.

La HV, Chu HD, Ha QT et al. (2022) SWEET gene family in sugar beet (Beta vulgaris): Genome-wide survey, phylogeny and expression analysis. Pakistan Journal of Biological Sciences 25 (5): 387-95.

Man Le T, Huyen Tran TT, Quyen Vu X et al. (2022) Genome-wide identification and analysis of genes encoding putative heat shock protein 70 in papaya (Carica papaya). Pakistan Journal of Biological Sciences 25 (6): 468-75. doi: 10.3923/pjbs.2022.468.475.

Khan AR, Mokhtar NI, Zainuddin Z et al. (2021) In silico characterization of UGT74G1 protein in Stevia rebaudiana Bertoni Accession MS007. Journal of Tropical Life Science 11 (3): 323-30. doi: 10.11594/jtls.1.1.%25x.

Hu B, Jin J, Guo A-Y et al. (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics (Oxford, England) 31 (8): 1296-7. doi: 10.1093/bioinformatics/btu817.

Larkin MA, Blackshields G, Brown NP et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23 (21): 2947-2948. doi: 10.1093/bioinformatics/btm404.

Kumar S, Stecher G, Li M et al. (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35 (6): 1547-1549. doi: 10.1093/molbev/msy096.

Briesemeister S, Rahnenfuhrer J, Kohlbacher O (2010) YLoc--an interpretable web server for predicting subcellular localization. Nucleic Acids Research 38 (Web Server issue):W497-502. doi: 10.1093/nar/gkq477.

Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95-8.

Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC et al. (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34 (12):3299-302. doi: 10.1093/molbev/msx248.

Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 (11): 1451-2.

Barrett T, Wilhite SE, Ledoux P et al. (2013) NCBI GEO: archive for functional genomics data sets - update. Nucleic Acids Research 41 (Database issue): D991-D995. doi: 10.1093/nar/gks1193.

Dash S, Cannon EKS, Kalberer SR et al. (2016) PeanutBase and other bioinformatic resources for peanut. In: Stalker HT, Wilson FR, eds. Peanuts: Genetics, processing, and utilization. AOCS Press: 241-252. doi: 10.1016/B978-1-63067-038-2.00008-3.

Clevenger J, Chu Y, Scheffler B, Ozias-Akins P. A Developmental Transcriptome Map for Allotetraploid Arachis hypogaea. Frontiers in Plant Science 2016; 7. doi: 10.3389/fpls.2016.01446.

Paul MJ, Watson A, Griffiths CA (2020) Trehalose 6-phosphate signalling and impact on crop yield. Biochemical Society Transaction 48 (5): 2127-2137. doi: 10.1042/bst20200286.

Paul MJ, Oszvald M, Jesus C et al. (2017) Increasing crop yield and resilience with trehalose 6-phosphate: targeting a feast–famine mechanism in cereals for better source–sink optimization. Journal of Experimental Botany 68(16):4455-62. doi: 10.1093/jxb/erx083.

Oszvald M, Primavesi LF, Griffiths CA et al. (2018) Trehalose 6-Phosphate Regulates Photosynthesis and Assimilate Partitioning in Reproductive Tissue. Plant Physiology 176 (4): 2623-2638. doi: 10.1104/pp.17.01673.

Vishal B, Krishnamurthy P, Ramamoorthy R, Kumar PP (2019) OsTPS8 controls yield-related traits and confers salt stress tolerance in rice by enhancing suberin deposition. New Phytologist 221 (3):1369-86. doi: 10.1111/nph.15464.

Lin Q, Yang J, Wang Q et al. (2019) Overexpression of the trehalose-6-phosphate phosphatase family gene AtTPPF improves the drought tolerance of Arabidopsis thaliana. BMC Plant Biology 19 (1): 381. doi: 10.1186/s12870-019-1986-5.

Lin Q, Wang S, Dao Y et al. (2020) Arabidopsis thaliana trehalose-6-phosphate phosphatase gene TPPI enhances drought tolerance by regulating stomatal apertures. Journal of Experimental Botany 71 (14): 4285-4297. doi: 10.1093/jxb/eraa173.