De novo gene integration into regulatory networks via interaction with conserved genes in peach

Yunpeng Cao , Jiayi Hong , Yun Zhao , Xiaoxu Li , Xiaofeng Feng , Han Wang , Lin Zhang , Mengfei Lin , Yongping Cai , Yuepeng Han

Horticulture Research ›› 2024, Vol. 11 ›› Issue (12) : 252

PDF (258KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (12) :252 DOI: 10.1093/hr/uhae252
Articles
research-article
De novo gene integration into regulatory networks via interaction with conserved genes in peach
Author information +
History +
PDF (258KB)

Abstract

De novo genes can evolve “from scratch” from noncoding sequences, acquiring novel functions in organisms and integrating into regulatory networks during evolution to drive innovations in important phenotypes and traits. However, identifying de novo genes is challenging, as it requires high-quality genomes from closely related species. According to the comparison with nine closely related Prunus genomes, we determined at least 178 de novo genes in P. persica “baifeng”. The distinct differences were observed between de novo and conserved genes in gene characteristics and expression patterns. Gene ontology enrichment analysis suggested that Type I de novo genes originated from sequences related to plastid modification functions, while Type II genes were inferred to have derived from sequences related to reproductive functions. Finally, transcriptome sequencing across different tissues and developmental stages suggested that de novo genes have been evolutionarily recruited into existing regulatory networks, playing important roles in plant growth and development, which was also supported by WGCNA analysis and quantitative trait loci data. This study lays the groundwork for future research on the origins and functions of genes in Prunus and related taxa.

Cite this article

Download citation ▾
Yunpeng Cao, Jiayi Hong, Yun Zhao, Xiaoxu Li, Xiaofeng Feng, Han Wang, Lin Zhang, Mengfei Lin, Yongping Cai, Yuepeng Han. De novo gene integration into regulatory networks via interaction with conserved genes in peach. Horticulture Research, 2024, 11 (12) : 252 DOI:10.1093/hr/uhae252

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

We sincerely thank Prof. Hui Song from Qingdao Agricultural University for his valuable suggestions on the identification of de novo genes. We also express our gratitude to the editors and reviewers for their insightful comments and thorough review of our manuscript. This research was funded by the National Natural Science Foundation of China (Grant No. U23A20206 and Grant No. 32201602), the Natural Science Fund of Hubei Province (Grant No. 2023AFB1036 and Grant No. 2022CFB932), the Beijing Life Science Academy Project (Grant No. 2023200CC0270), the Key Special Project of Intergovernmental International Cooperation of the National Key R&D Program of China (Grant No. 2023YFE0125100), the Knowledge Innovation Program of Wuhan Basic Research (Grant No. 2022020801010167), and the China Agriculture Research System (Grant No. CARS-30).

Author contributions

Y.P.C. and Y.P.H. spearheaded the conception and design of the study. Y.P.C. was responsible for data analysis, drafting the manuscript, and incorporating revisions. Collaborative data analyses were performed by Y.P.C., J.Y.H., L.Z., X.X.L., X.F.F., H.W., L.Z., M.F.L., and Y.P.C. Both Y.P.C. and Y.P.H. critically reviewed and assessed the final manuscript.

Data availability

The RNA-seq project of peach (P. persica) has been deposited at the BIG Data Center (https://bigd.big.ac.cn/gsa) under the accession: PRJCA011988.

Conflict of Interests Statement

The authors declare that they have no competing interests.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1]

Chen S, Krinsky BH, Long M. New genes as drivers of phenotypic evolution. Nat Rev Genet. 2013; 14:645-60

[2]

Jiang L, Li X, Lyu K. et al. Rosaceae phylogenomic studies provide insights into the evolution of new genes. Hortic Plant J. 2024

[3]

Kaessmann H. Origins, evolution, and phenotypic impact of new genes. Genome Res. 2010; 20:1313-26

[4]

Long M, Betrán E, Thornton K. et al. The origin of new genes: glimpses from the young and old. Nat Rev Genet. 2003; 4:865-75

[5]

Parikh SB, Houghton C, Van Oss SB. et al. Origins, evolution, and physiological implications of de novo genes in yeast. Yeast. 2022; 39:471-81

[6]

Wang Y-W, Hess J, Slot JC. et al. De novo gene birth, horizontal gene transfer, and gene duplication as sources of new gene families associated with the origin of symbiosis in amanita. Genome Biol Evol. 2020; 12:2168-82

[7]

Van Oss SB, Carvunis A-R. De novo gene birth. PLoS Genet. 2019; 15:e1008160

[8]

Cridland JM, Majane AC, Zhao L. et al. Population biology of accessory gland-expressed de novo genes in Drosophila melanogaster. Genetics. 2022; 220:

[9]

Song H, Guo Z, Zhang X. et al. De novo genes in Arachis hypogaea cv. Tifrunner: systematic identification, molecular evolution, and potential contributions to cultivated peanut. Plant J. 2022; 111:1081-95

[10]

Weisman CM. The origins and functions of de novo genes: against all odds? J Mol Evol. 2022; 90:244-57

[11]

Schmitz JF, Ullrich KK, Bornberg-Bauer E. Incipient de novo genes can evolve from frozen accidents that escaped rapid transcript turnover. Nat Ecol Evol. 2018; 2:1626-32

[12]

Vakirlis N, Hebert AS, Opulente DA. et al. A molecular portrait of de novo genes in yeasts. Mol Biol Evol. 2018; 35:631-45

[13]

Bornberg-Bauer E, Heames B. Becoming a de novo gene. Nature Ecolo Evol. 2019; 3:524-5

[14]

An NA, Zhang J, Mo F. et al. De novo genes with an lncRNA origin encode unique human brain developmental functionality. Nat Ecol Evol. 2023; 7:264-78

[15]

Poretti M, Praz CR, Sotiropoulos AG. et al. A survey of lineage-specific genes in Triticeae reveals de novo gene evolution from genomic raw material. Plant Direct. 2023; 7:e484

[16]

Zhang L, Ren Y, Yang T. et al. Rapid evolution of protein diversity by de novo origination in Oryza. Nat Ecol Evol. 2019; 3:679-90

[17]

Gubala AM, Schmitz JF, Kearns MJ. et al. The Goddard and saturn genes are essential for drosophila male fertility and may have arisen de novo. Mol Biol Evol. 2017; 34:1066-82

[18]

Guerzoni D, McLysaght A. De novo origins of human genes. PLoS Genet. 2011; 7:e1002381

[19]

Peng J, Zhao L. The origin and structural evolution of de novo genes in drosophila. Nat Commun. 2024; 15:810

[20]

Levine MT, Jones CD, Kern AD. et al. Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression. Proc Natl Acad Sci. 2006; 103:9935-9

[21]

Begun DJ, Lindfors HA, Thompson ME. et al. Recently evolved genes identified from Drosophila yakuba and D. erecta accessory gland expressed sequence tags. Genetics. 2006; 172:1675-81

[22]

Cai J, Zhao R, Jiang H. et al. De novo origination of a new protein-coding gene in Saccharomyces cerevisiae. Genetics. 2008; 179:487-96

[23]

Chen S, Zhang YE, Long M. Long M: new genes in drosophila quickly become essential. Science. 2010; 330:1682-5

[24]

Zhou Q, Zhang G, Zhang Y. et al. On the origin of new genes in drosophila. Genome Res. 2008; 18:1446-55

[25]

Zhao L, Saelao P, Jones CD. et al. Origin and spread of de novo genes in Drosophila melanogaster populations. Science. 2014; 343:769-72

[26]

Knowles DG, McLysaght A. Recent de novo origin of human protein-coding genes. Genome Res. 2009; 19:1752-9

[27]

Carvunis A-R, Rolland T, Wapinski I. et al. Proto-genes and de novo gene birth. Nature. 2012; 487:370-4

[28]

Ruiz-Orera J, Verdaguer-Grau P, Villanueva-Cañas JL. et al. Translation of neutrally evolving peptides provides a basis for de novo gene evolution. Nat Ecol Evol. 2018; 2:890-6

[29]

Rivard EL, Ludwig AG, Patel PH. et al. A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster. PLoS Genet. 2021; 17:e1009787

[30]

McLysaght A, Hurst LD. Open questions in the study of de novo genes: what, how and why. Nat Rev Genet. 2016; 17:567-78

[31]

Vakirlis N, Acar O, Hsu B. et al. De novo emergence of adaptive membrane proteins from thymine-rich genomic sequences. Nat Commun. 2020; 11:781

[32]

Li Z-W, Chen X, Wu Q. et al. On the origin of de novo genes in Arabidopsis thaliana populations. Genome Biol Evol. 2016; 8:2190-202

[33]

Jin G, Ma P-F, Wu X. et al. New genes interacted with recent whole-genome duplicates in the fast stem growth of bamboos. Mol Biol Evol. 2021; 38:5752-68

[34]

Qi M, Zheng W, Zhao X. et al. QQS orphan gene and its interactor NF-YC 4 reduce susceptibility to pathogens and pests. Plant Biotechnol J. 2019; 17:252-63

[35]

Li L, Foster CM, Gan Q. et al. Identification of the novel protein QQS as a component of the starch metabolic network in Arabidopsis leaves. Plant J. 2009; 58:485-98

[36]

Xiao W, Liu H, Li Y. et al. A rice gene of de novo origin negatively regulates pathogen-induced defense response. PLoS One. 2009; 4:e4603

[37]

Chen R, Xiao N, Lu Y. et al. A de novo evolved gene contributes to rice grain shape difference between indica and japonica. Nat Commun. 2023; 14:5906

[38]

Cao K, Peng Z, Zhao X. et al. Chromosome-level genome assemblies of four wild peach species provide insights into genome evolution and genetic basis of stress resistance. BMC Biol. 2022; 20:139

[39]

Zhou P, Lei S, Zhang X. et al. Genome sequencing revealed the red-flower trait candidate gene of a peach landrace. Hortic Res. 2023; 10:

[40]

Li X, Wang J, Su M. et al. Multiple-statistical genome-wide association analysis and genomic prediction of fruit aroma and agronomic traits in peaches. Hortic Res. 2023; 10:

[41]

International Peach Genome Initiative, Verde I, Abbott AG. et al. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet. 2013; 45:487-94

[42]

Cao K, Yang X, Li Y. et al. New high-quality peach (Prunus persica L. Batsch) genome assembly to analyze the molecular evolutionary mechanism of volatile compounds in peach fruits. Plant J. 2021; 108:281-95

[43]

Tan Q, Li S, Zhang Y. et al. Chromosome-level genome assemblies of five Prunus species and genome-wide association studies for key agronomic traits in peach. Hortic Res. 2021; 8:213

[44]

Zheng T, Li P, Zhuo X. et al. The chromosome-level genome provides insight into the molecular mechanism underlying the tortuous-branch phenotype of Prunus mume. New Phytol. 2022; 235:141-56

[45]

Fang ZZ, Lin-Wang K, Dai H. et al. The genome of low-chill Chinese plum “Sanyueli”(Prunus salicina Lindl.) provides insights into the regulation of the chilling requirement of flower buds. Mol Ecol Resour. 2022; 22:1919-38

[46]

Zhang W, Gao Y, Long M. et al. Origination and evolution of orphan genes and de novo genes in the genome of Caenorhabditis elegans. Sci China Life Sci. 2019; 62:579-93

[47]

Neme R, Tautz D. Phylogenetic patterns of emergence of new genes support a model of frequent de novo evolution. BMC Genomics. 2013; 14:117-3

[48]

Wolf YI, Novichkov PS, Karev GP. et al. The universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages. Proc Natl Acad Sci. 2009; 106:7273-80

[49]

Wu D-D, Irwin DM, Zhang Y-P. De novo origin of human protein-coding genes. PLoS Genet. 2011; 7:e1002379

[50]

Zhang RX, Liu Y, Zhang X. et al. Two adjacent NAC transcription factors regulate fruit maturity date and flavor in peach. New Phytol. 2024; 241:632-49

[51]

Cao Y, Mo W, Li Y. et al. Functional characterization of NBS-LRR genes reveals an NBS-LRR gene that mediates resistance against Fusarium wilt. BMC Biol. 2024; 22:45

[52]

An J-P, Zhao L, Cao Y-P. et al. The SMXL8-AGL9 module mediates crosstalk between strigolactone and gibberellin to regulate strigolactone-induced anthocyanin biosynthesis in apple. Plant Cell. 2024;koae191

[53]

Wittkopp PJ, Kalay G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet. 2012; 13:59-69

[54]

Shahmuradov IA, Solovyev VV. Nsite, NsiteH and NsiteM computer tools for studying transcription regulatory elements. Bioinformatics. 2015; 31:3544-5

[55]

Lescot M, Déhais P, Thijs G. et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002; 30:325-7

[56]

Begun DJ, Lindfors HA, Kern AD. et al. Evidence for de novo evolution of testis-expressed genes in the drosophila yakuba/Drosophila erecta clade. Genetics. 2007; 176:1131-7

[57]

Zhang W, Landback P, Gschwend AR. et al. New genes drive the evolution of gene interaction networks in the human and mouse genomes. Genome Biol. 2015; 16:1-14

[58]

Zhang B, Horvath S. A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol. 2005; 4:

[59]

Lambert P, Campoy JA, Pacheco I. et al. Identifying SNP markers tightly associated with six major genes in peach [Prunus persica (L.) Batsch] using a high-density SNP array with an objective of marker-assisted selection (MAS). Tree Genet Genomes. 2016; 12:1-21

[60]

Shi P, Xu Z, Zhang S. et al. Construction of a high-density SNP-based genetic map and identification of fruit-related QTLs and candidate genes in peach [Prunus persica (L.) Batsch]. BMC Plant Biol. 2020; 20:1-16

[61]

Yamamoto T, Shimada T, Imai T. et al. Characterization of morphological traits based on a genetic linkage map in peach. Breed Sci. 2001; 51:271-8

[62]

Rawandoozi ZJ, Hartmann TP, Carpenedo S. et al. Mapping and characterization QTLs for phenological traits in seven pedigree-connected peach families. BMC Genomics. 2021; 22:1-16

[63]

Dirlewanger E, Cosson P, Boudehri K. et al. Development of a second-generation genetic linkage map for peach [Prunus persica (L.) Batsch] and characterization of morphological traits affecting flower and fruit. Tree Genet Genomes. 2006; 3:1-13

[64]

Martínez-García PJ, Parfitt DE, Ogundiwin EA. et al. High density SNP mapping and QTL analysis for fruit quality characteristics in peach (Prunus persica L.). Tree Genet Genomes. 2013; 9:19-36

[65]

Zeballos JL, Abidi W, Giménez R. et al. Mapping QTLs associated with fruit quality traits in peach [Prunus persica (L.) Batsch] using SNP maps. Tree Genet Genomes. 2016; 12:1-17

[66]

Bliss FA, Arulsekar S, Foolad MR. et al. An expanded genetic linkage map of Prunus based on an interspecific cross between almond and peach. Genome. 2002; 45:520-9

[67]

Ogundiwin EA, Peace CP, Gradziel TM. et al. A fruit quality gene map of Prunus. BMC Genomics. 2009; 10:587-13

[68]

Serra O, Giné-Bordonaba J, Eduardo I. et al. Genetic analysis of the slow-melting flesh character in peach. Tree Genet Genomes. 2017; 13:1-13

[69]

Pacheco I, Bassi D, Eduardo I. et al. QTL mapping for brown rot (Monilinia fructigena) resistance in an intraspecific peach (Prunus persica L. Batsch) F1 progeny. Tree Genet Genomes. 2014; 10:1223-42

[70]

Rawandoozi ZJ, Hartmann TP, Carpenedo S. et al. Identification and characterization of QTLs for fruit quality traits in peach through a multi-family approach. BMC Genomics. 2020; 21:1-18

[71]

Sauge M-H, Lambert P, Pascal T. Co-localisation of host plant resistance QTLs affecting the performance and feeding behaviour of the aphid Myzus persicae in the peach tree. Heredity. 2012; 108:292-301

[72]

Blaker KM, Chaparro JX, Beckman TG. Identification of QTLs controlling seed dormancy in peach (Prunus persica). Tree Genet Genomes. 2013; 9:659-68

[73]

Duval H, Hoerter M, Polidori J. et al. High-resolution mapping of the RMia gene for resistance to root-knot nematodes in peach. Tree Genet Genomes. 2014; 10:297-306

[74]

Rajapakse S, Belthoff LE, He G. et al. Genetic linkage mapping in peach using morphological, RFLP and RAPD markers. Theor Appl Genet. 1995; 90:503-10

[75]

Wang Y, Georgi LL, Reighard GL. et al. Genetic mapping of the evergrowing gene in peach [Prunus persica (L.) Batsch]. J Hered. 2002; 93:352-8

[76]

Decroocq V, Foulongne M, Lambert P. et al. Analogues of virus resistance genes map to QTLs for resistance to sharka disease in Prunus davidiana. Mol Gen Genomics. 2005; 272:680-9

[77]

Verde I, Quarta R, Cedrola C. et al. QTL analysis of agronomic traits in a BC 1 peach population. Acta Hortic. 2002;291-7

[78]

Zhebentyayeva TN, Fan S, Chandra A. et al. Dissection of chilling requirement and bloom date QTLs in peach using a whole genome sequencing of sibling trees from an F 2 mapping population. Tree Genet Genomes. 2014; 10:35-51

[79]

Fan S, Bielenberg DG, Zhebentyayeva TN. et al. Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytol. 2010; 185:917-30

[80]

Desnoues E, Baldazzi V, Génard M. et al. Dynamic QTLs for sugars and enzyme activities provide an overview of genetic control of sugar metabolism during peach fruit development. J Exp Bot. 2016; 67:3419-31

[81]

Dhanapal AP, Martínez-García PJ, Gradziel TM. et al. First genetic linkage map of chilling injury susceptibility in peach (Prunus persica (L.) Batsch) fruit with SSR and SNP markers. J Plant Sci Mol Breed. 2012; 1:

[82]

Nuñez-Lillo G, Cifuentes-Esquivel A, Troggio M. et al. Identification of candidate genes associated with mealiness and maturity date in peach [Prunus persica (L.) Batsch] using QTL analysis and deep sequencing. Tree Genet Genomes. 2015; 11:1-13

[83]

Yang N, Reighard G, Ritchie D. et al. Mapping quantitative trait loci associated with resistance to bacterial spot (Xanthomonas arboricola pv. Pruni) in peach. Tree Genet Genomes. 2013; 9:573-86

[84]

Bielenberg DG, Rauh B, Fan S. et al. Wells CE: genotyping by sequencing for SNP-based linkage map construction and QTL analysis of chilling requirement and bloom date in peach [Prunus persica (L.) Batsch]. PLoS One. 2015; 10:e0139406

[85]

da Silva LC, Bassi D, Bianco L. et al. Genetic dissection of fruit weight and size in an F 2 peach (Prunus persica (L.) Batsch) progeny. Mol Breed. 2015; 35:1-19

[86]

da Silva LC, Cai L, Fu W. et al. Multi-locus genome-wide association studies reveal fruit quality hotspots in peach genome. Front Plant Sci. 2021; 12:12

[87]

Abrusán G. Integration of new genes into cellular networks,and their structural maturation. Genetics. 2013; 195:1407-17

[88]

Cui X, Lv Y, Chen M. et al. Young genes out of the male: an insight from evolutionary age analysis of the pollen transcriptome. Mol Plant. 2015; 8:935-45

[89]

Yang Z, Huang J. De novo origin of new genes with introns in Plasmodium vivax. FEBS Lett. 2011; 585:641-4

[90]

Vishnoi A, Kryazhimskiy S, Bazykin GA. et al. Young proteins experience more variable selection pressures than old proteins. Genome Res. 2010; 20:1574-81

[91]

Rödelsperger C, Prabh N, Sommer RJ. New gene origin and deep taxon phylogenomics: opportunities and challenges. Trends Genet. 2019; 35:914-22

[92]

Durand É, Gagnon-Arsenault I, Hallin J. et al. Turnover of ribosome-associated transcripts from de novo ORFs produces gene-like characteristics available for de novo gene emergence in wild yeast populations. Genome Res. 2019; 29:932-43

[93]

Teichmann SA, Babu MM. Gene regulatory network growth by duplication. Nat Genet. 2004; 36:492-6

[94]

Papp B, Pál C, Hurst LD. Evolution of cis-regulatory elements in duplicated genes of yeast. Trends Genet. 2003; 19:417-22

[95]

He BZ, Holloway AK, Maerkl SJ. et al. Does positive selection drive transcription factor binding site turnover? A test with drosophila cis-regulatory modules. PLoS Genet. 2011; 7:e1002053

[96]

Tsai ZT-Y, Tsai H-K, Cheng J-H. et al. Wang D: evolution of cis-regulatory elements in yeast de novo and duplicated new genes. BMC Genomics. 2012; 13:1-12

[97]

Takeda T, Shirai K, Kim YW. et al. A de novo gene originating from the mitochondria controls floral transition in Arabidopsis thaliana. Plant Mol Biol. 2023; 111:189-203

[98]

Berg OG, Kurland CG. Why mitochondrial genes are most often found in nuclei. Mol Biol Evol. 2000; 17:951-61

[99]

O’Conner S, Li L. Mitochondrial fostering: the mitochondrial genome may play a role in plant orphan gene evolution. Front Plant Sci. 2020; 11:600117

[100]

Noutsos C, Kleine T, Armbruster U. et al. Nuclear insertions of organellar DNA can create novel patches of functional exon sequences. Trends Genet. 2007; 23:597-601

[101]

Christensen AC. Plant mitochondrial genome evolution can be explained by DNA repair mechanisms. Genome Biol Evol. 2013; 5:1079-86

[102]

Zhang J-Y, Zhou Q. On the regulatory evolution of new genes throughout their life history. Mol Biol Evol. 2019; 36:15-27

[103]

Wu B, Knudson A. Tracing the de novo origin of protein-coding genes in yeast. MBio. 2018; 9:10-1128

[104]

Bekpen C, Xie C, Tautz D. Dealing with the adaptive immune system during de novo evolution of genes from intergenic sequences. BMC Evol Biol. 2018; 18:1-11

[105]

Donoghue MTA, Keshavaiah C, Swamidatta SH. et al. Evolutionary origins of Brassicaceae specific genes in Arabidopsis thaliana. BMC Evol Biol. 2011; 11:1-23

[106]

Heinen TJAJ, Staubach F, Häming D. et al. Emergence of a new gene from an intergenic region. Curr Biol. 2009; 19:1527-31

[107]

Jiang L, Lin M, Wang H. et al. Haplotype-resolved genome assembly of Bletilla striata (Thunb.) Reichb. f. To elucidate medicinal value. Plant J. 2022; 111:1340-53

[108]

Pertea M, Kim D, Pertea GM. et al. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc. 2016; 11:1650-67

[109]

Pertea G, Pertea M. GFF utilities: GffRead and GffCompare. F1000Res. 2020; 9:304

[110]

Pinosio S, Marroni F, Zuccolo A. et al. A draft genome of sweet cherry (Prunus avium L.) reveals genome-wide and local effects of domestication. Plant J. 2020; 103:1420-32

[111]

Lian X, Zhang H, Jiang C. et al. De novo chromosome-level genome of a semi-dwarf cultivar of Prunus persica identifies the aquaporin PpTIP 2 as responsible for temperature-sensitive semi-dwarf trait and PpB3-1 for flower type and size. Plant Biotechnol J. 2022; 20:886-902

[112]

Altschul SF, Madden TL, Schäffer AA. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997; 25:3389-402

[113]

Kent WJ. BLAT—the BLAST-like alignment tool. Genome Res. 2002; 12:656-64

[114]

Chen C, Chen H, Zhang Y. et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13:1194-202

[115]

Ikemura T. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Mol Biol. 1981; 151:389-409

[116]

Mészáros B, Erd˝os G, Dosztányi Z. IUPred2A: context-dependent prediction of protein disorder as a function of redox state and protein binding. Nucleic Acids Res. 2018; 46:W329-37

[117]

Jin J, Tian F, Yang D-C. et al. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 2017; 45:D1040-5

[118]

Huerta-Cepas J, Forslund K, Coelho LP. et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol. 2017; 34:2115-22

[119]

Wu T, Hu E, Xu S. et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation (Camb). 2021; 2:100141

[120]

Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008; 9:1-13

PDF (258KB)

89

Accesses

0

Citation

Detail

Sections
Recommended

/