Online First

 Preview Page

Research Article

Genome-Wide Characterization and Evolutionary Conservation of the Mildew Locus O Gene Family in Coffea Species Reveal Candidate Powdery Mildew Susceptibility Genes
Mi Kwon1†
,
Junseok Lee1†
,
Junhyeop Sung1
,
Myung-Shin Kim1*
1Department of Biosciences and Bioinformatics, Myongji University, Yongin 17058, Korea
*Corresponding Author
†These authors contributed equally to this work.
PDF XML Citation
Abstract

Coffee (Coffea spp.) represents a high-value perennial crop globally, yet its productivity is increasingly threatened by pathogens such as powdery mildew (PM). While PM resistance is often achieved through loss-of-function mutations in Mildew Locus O (MLO) susceptibility genes, these have remained poorly explored in coffee despite the recent availability of high-quality chromosome-level genome assemblies. A total of 90 MLO genes were identified across the four Coffea genomes and classified into seven major phylogenetic clades. Notably, six members of the Clade V-ii subgroup, orthologous to known PM susceptibility factors, exhibited exceptional sequence and three-dimensional structural conservation supported by AlphaFold3 modeling. These candidates were characterized by conserved C-terminal motifs, including a DFSF consensus sequence as well as specific enrichment of defense-related cis-regulatory elements, in this case TC-rich repeats, within their promoter regions. These findings highlight their potential utility as molecular targets for resistance breeding and genome-editing strategies in coffee improvement programs. This study provides comprehensive insights into the evolutionary conservation of the MLO gene family in Coffea species and identifies candidate susceptibility-associated genes for PM resistance.

Keywords
Coffeaarabica
Coffeacanephora
Coffeaeugenioides
gene family evolution
MLO
References
1

Abramson J, Adler J, Dunger J, Evans R, Green T, Pritzel A, Ronneberger O, Willmore L, Ballard AJ, et al. (2024) Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature 630:493-500. https://doi.org/10.1038/s41586-024-07487-w

10.1038/s41586-024-07487-w38718835PMC11168924
2

Acevedo-Garcia J, Gruner K, Reinstädler A, Kemen A, Kemen E, Cao L, Takken FLW, Reitz MU, Schäfer P, et al. (2017) The powdery mildew-resistant Arabidopsismlo2 mlo6 mlo12 triple mutant displays altered infection phenotypes with diverse types of phytopathogens. Sci Rep 7:9319. https://doi.org/10.1038/s41598-017-07188-7

10.1038/s41598-017-07188-728839137PMC5570895
3

Acevedo-Garcia J, Kusch S, Panstruga R (2014) Magical mystery tour: MLO proteins in plant immunity and beyond. New Phytol 204:273-281. https://doi.org/10.1111/nph.12889

10.1111/nph.12889
4

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402. https://doi.org/10.1093/nar/25.17.3389

10.1093/nar/25.17.33899254694PMC146917
5

Andolfo G, Iovieno P, Ricciardi L, Lotti C, Filippone E, Pavan S, Ercolano MR (2019) Evolutionary conservation of MLO gene promoter signatures. BMC Plant Biol 19:150. https://doi.org/10.1186/s12870-019-1749-3

10.1186/s12870-019-1749-330995906PMC6471879
6

Bai Y, Pavan S, Zheng Z, Zappel NF, Reinstädler A, Lotti C, De Giovanni C, Ricciardi L, Lindhout P, et al. (2008) Naturally occurring broad-spectrum powdery mildew resistance in a central American tomato accession is caused by loss of mlo function. Mol Plant Microbe Interact 21:30-39. https://doi.org/10.1094/MPMI-21-1-0030

10.1094/MPMI-21-1-0030
7

Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Res 43:W39-W49. https://doi.org/10.1093/nar/gkv416

10.1093/nar/gkv41625953851PMC4489269
8

Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The Protein Data Bank. Nucleic Acids Res 28:235-242. https://doi.org/10.1093/nar/28.1.235

10.1093/nar/28.1.23510592235PMC102472
9

Bunn C, Läderach P, Ovalle Rivera O, Kirschke D (2015) A bitter cup: climate change profile of global production of Arabica and Robusta coffee. Clim Change 129:89-101. https://doi.org/10.1007/s10584-014-1306-x

10.1007/s10584-014-1306-x
10

Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, et al. (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695-705. https://doi.org/10.1016/S0092-8674(00)81912-1

10.1016/S0092-8674(00)81912-1
11

Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972-1973. https://doi.org/10.1093/bioinformatics/btp348

10.1093/bioinformatics/btp34819505945PMC2712344
12

Chen Z, Hartmann HA, Wu MJ, Friedman EJ, Chen JG, Pulley M, Schulze-Lefert P, Panstruga R, Jones AM (2006) Expression analysis of the AtMLO gene family encoding plant-specific seven-transmembrane domain proteins. Plant Mol Biol 60:583-597. https://doi.org/10.1007/s11103-005-5082-x

10.1007/s11103-005-5082-x
13

Chen Z, Noir S, Kwaaitaal M, Hartmann HA, Wu MJ, Mudgil Y, Sukumar P, Muday G, Panstruga R, et al. (2009) Two seven-transmembrane domain MILDEW RESISTANCE LOCUS O proteins cofunction in Arabidopsis root thigmomorphogenesis. Plant Cell 21:1972-1991. https://doi.org/10.1105/tpc.108.062653

10.1105/tpc.108.06265319602625PMC2729597
14

Chou KC, Shen HB (2010) Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS One 5:e11335. https://doi.org/10.1371/journal.pone.0011335

10.1371/journal.pone.001133520596258PMC2893129
15

Clarindo WR, Carvalho CR, Caixeta ET, Koehler AD (2013) Following the track of “Híbrido de Timor” origin by cytogenetic and flow cytometry approaches. Genet Resour Crop Evol 60:2253-2259. https://doi.org/10.1007/s10722-013-9990-3

10.1007/s10722-013-9990-3
16

Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, Westphal L, Vogel J, Lipka V, Kemmerling B, et al. (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38:716-720. https://doi.org/10.1038/ng1806

10.1038/ng1806
17

Davis AP (2011) Psilanthus mannii, the type species of Psilanthus, transferred to Coffea. Nord J Bot 29:471-472. https://doi.org/10.1111/j.1756-1051.2011.01113.x

10.1111/j.1756-1051.2011.01113.x
18

Davis TC, Jones DS, Dino AJ, Cejda NI, Yuan J, Willoughby AC, Kessler SA (2017) Arabidopsis thaliana MLO genes are expressed in discrete domains during reproductive development. Plant Reprod 30:185-195. https://doi.org/10.1007/s00497-017-0313-2

10.1007/s00497-017-0313-2
19

de Souza SJ, Long M, Gilbert W (1996) Introns and gene evolution. Genes Cells 1:493-505. https://doi.org/10.1046/j.1365-2443.1996.d01-264.x

10.1046/j.1365-2443.1996.d01-264.x
20

Denoeud F, Carretero-Paulet L, Dereeper A, Droc G, Guyot R, Pietrella M, Zheng C, Alberti A, Anthony F, et al. (2014) The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345:1181-1184. https://doi.org/10.1126/science.1255274

10.1126/science.1255274
21

Fondevilla S, Rubiales D (2012) Powdery mildew control in pea: a review. Agron Sustain Dev 32:401-409. https://doi.org/10.1007/s13593-011-0033-1

10.1007/s13593-011-0033-1
22

Food and Agriculture Organization of the United Nations (FAO) (2025) Adverse climatic conditions drive coffee prices to highest level in years. https://www.fao.org/newsroom/detail/adverse-climatic-conditions-drive-coffee-prices-to-highest-level-in-years/en. Accessed 10 Mar 2026

23

Garretón V, Carpinelli J, Jordana X, Holuigue L (2002) The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol 130:1516-1526. https://doi.org/10.1104/pp.009886

10.1104/pp.00988612428016PMC166670
24

Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784-3788. https://doi.org/10.1093/nar/gkg563

10.1093/nar/gkg56312824418PMC168970
25

Glawe DA (2008) The powdery mildews: A review of the world’s most familiar (yet poorly known) plant pathogens. Annu Rev Phytopathol 46:27-51. https://doi.org/10.1146/annurev.phyto.46.081407.104740

10.1146/annurev.phyto.46.081407.104740
26

Hacquard S (2014) The genomics of powdery mildew fungi: past achievements, present status and future prospects. Adv Bot Res 70:109-142. https://doi.org/10.1016/B978-0-12-397940-7.00004-5

10.1016/B978-0-12-397940-7.00004-5
27

Harris CR, Millman KJ, van der Walt SJ, Gommers R, Virtanen P, Cournapeau D, Wieser E, Taylor J, Berg S, et al. (2020) Array programming with NumPy. Nature 585:357-362. https://doi.org/10.1038/s41586-020-2649-2

10.1038/s41586-020-2649-232939066PMC7759461
28

Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217-218:109-119. https://doi.org/10.1016/j.plantsci.2013.12.007

10.1016/j.plantsci.2013.12.007
29

Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci U S A 96:15348-15353. https://doi.org/10.1073/pnas.96.26.15348

10.1073/pnas.96.26.1534810611387PMC24822
30

Hunter JD (2007) Matplotlib: a 2D graphics environment. Comput Sci Eng 9:90-95. https://doi.org/10.1109/MCSE.2007.55

10.1109/MCSE.2007.55
31

Hussain B, Raza Q, Ramzan H, Awan MF, Budak H, Ali Z, Atif RM (2025) Genome-wide characterization highlights key roles for bread wheat MLO genes in powdery mildew and abiotic stresses. Rice 18:8. https://doi.org/10.1186/s12284-025-00832-1

10.1186/s12284-025-00832-141042422PMC12494513
32

International Coffee Organization (ICO) (2018) Development of coffee trade flows. https://ico.org/documents/cy2017-18/icc-121-4e-trade-flows.pdf. Accessed 10 Mar 2026

33

Jones DS, Yuan J, Smith BE, Willoughby AC, Kumimoto EL, Kessler SA (2017) MILDEW RESISTANCE LOCUS O function in pollen tube reception is linked to its oligomerization and subcellular distribution. Plant Physiol 175:172-185. https://doi.org/10.1104/pp.17.00523

10.1104/pp.17.0052328724621PMC5580752
34

Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, et al. (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236-1240. https://doi.org/10.1093/bioinformatics/btu031

10.1093/bioinformatics/btu03124451626PMC3998142
35

Kalyaanamoorthy S, Minh BQ, Wong TKF, Von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587-589. https://doi.org/10.1038/nmeth.4285

10.1038/nmeth.428528481363PMC5453245
36

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772-780. https://doi.org/10.1093/molbev/mst010

10.1093/molbev/mst01023329690PMC3603318
37

Keren H, Lev-Maor G, Ast G (2010) Alternative splicing and evolution: diversification, exon definition and function. Nat Rev Genet 11:345-355. https://doi.org/10.1038/nrg2776

10.1038/nrg2776
38

Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330:968-971. https://doi.org/10.1126/science.1195211

10.1126/science.1195211
39

Kim MC, Lee SH, Kim JK, Chun HJ, Choi MS, Chung WS, Moon BC, Kang CH, Park CY, et al. (2002a) Mlo, a modulator of plant defense and cell death, is a novel calmodulin-binding protein: isolation and characterization of a rice Mlo homologue. J Biol Chem 277:19304-19314. https://doi.org/10.1074/jbc.M108478200

10.1074/jbc.M108478200
40

Kim MC, Panstruga R, Elliott C, Müller J, Devoto A, Yoon HW, Park HC, Cho MJ, Schulze-Lefert P (2002b) Calmodulin interacts with MLO protein to regulate defense against mildew in barley. Nature 416:447-451. https://doi.org/10.1038/416447a

10.1038/416447a
41

Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567-580. https://doi.org/10.1006/jmbi.2000.4315

10.1006/jmbi.2000.4315
42

Kusch S, Panstruga R (2017) mlo-based resistance: an apparently universal weapon to defeat powdery mildew disease. Mol Plant Microbe Interact 30:179-189. https://doi.org/10.1094/MPMI-12-16-0255-CR

10.1094/MPMI-12-16-0255-CR
43

Kusch S, Pesch L, Panstruga R (2016) Comprehensive phylogenetic analysis sheds light on the diversity and origin of the MLO family of integral membrane proteins. Genome Biol Evol 8:878-895. https://doi.org/10.1093/gbe/evw036

10.1093/gbe/evw03626893454PMC4824068
44

Lashermes P, Combes M-C, Robert J, Trouslot P, D’hont A, Anthony F, Charrier A (1999) Molecular characterisation and origin of the Coffea arabica L. genome. Mol Gene Genet 261:259-266. https://doi.org/10.1007/s004380050965

10.1007/s004380050965
45

Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325-327. https://doi.org/10.1093/nar/30.1.325

10.1093/nar/30.1.32511752327PMC99092
46

Letunic I, Bork P (2024) Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res 52:W78-W82. https://doi.org/10.1093/nar/gkae268

10.1093/nar/gkae26838613393PMC11223838
47

Liu Q, Zhu H (2008) Molecular evolution of the MLO gene family in Oryza sativa and their functional divergence. Gene 409:1-10. https://doi.org/10.1016/j.gene.2007.10.031

10.1016/j.gene.2007.10.031
48

Lyu H, Song J, Yin Y, Wang ML, Matsumoto T, Annabhemoju V, Meinhardt LW, Park S, Lim S, et al. (2025) A chromosome-level genome assembly of Coffea arabica L. var. ‘Kona Typica’. Sci Data 12:1314. https://doi.org/10.1038/s41597-025-05658-6

10.1038/s41597-025-05658-640730557PMC12307819
49

Marand AP, Eveland AL, Kaufmann K, Springer NM (2023) cis-regulatory elements in plant development, adaptation, and evolution. Annu Rev Plant Biol 74:111-137. https://doi.org/10.1146/annurev-arplant-070122-030236

10.1146/annurev-arplant-070122-03023636608347PMC9881396
50

McKinney W (2010) Data structures for statistical computing in Python. In: Proceedings of the 9th Python in Science Conference. pp 51-56. https://doi.org/10.25080/Majora-92bf1922-00a

10.25080/Majora-92bf1922-00a
51

Medrano JF, Cantu D, Minio A, Dreischer C, Gibbons T, Chin J, Chen S, Van Deynze A, Hulse-Kemp AM (2025) De novo whole-genome assembly and annotation of Coffea arabica var. Geisha, a high-quality coffee variety from the primary origin of coffee. G3 (Bethesda) 15:jkae262. https://doi.org/10.1093/g3journal/jkae262

10.1093/g3journal/jkae26239545517PMC11708220
52

Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Von Haeseler A, Lanfear R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530-1534. https://doi.org/10.1093/molbev/msaa015

10.1093/molbev/msaa01532011700PMC7182206
53

Moffett P (2009) Mechanisms of recognition in dominant R gene mediated resistance. Adv Virus Res 75:1-229. https://doi.org/10.1016/S0065-3527(09)07501-0

10.1016/S0065-3527(09)07501-0
54

Murthy PS, Madhava Naidu M (2012) Sustainable management of coffee industry by-products and value addition - A review. Resour Conserv Recycl 66:45-58. https://doi.org/10.1016/j.resconrec.2012.06.005

10.1016/j.resconrec.2012.06.005
55

Naeem S, Wang Y, Han S, Haider MZ, Sami A, Shafiq M, Ali Q, Bhatti MHT, Ahmad A, et al. (2024) Genome-wide analysis and identification of carotenoid cleavage oxygenase (CCO) gene family in coffee (Coffea arabica) under abiotic stress. BMC Genom Data 25:71. https://doi.org/10.1186/s12863-024-01248-4

10.1186/s12863-024-01248-439030545PMC11264761
56

Nekrasov V, Wang C, Win J, Lanz C, Weigel D, Kamoun S (2017) Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci Rep 7:482. https://doi.org/10.1038/s41598-017-00578-x

10.1038/s41598-017-00578-x28352080PMC5428673
57

Nguyen VNT, Vo KTX, Park H, Jeon JS, Jung KH (2016) A systematic view of the MLO family in rice suggests their novel roles in morphological development, diurnal responses, the light-signaling pathway, and various stress responses. Front Plant Sci 7:1413. https://doi.org/10.3389/fpls.2016.01413

10.3389/fpls.2016.0141327729915PMC5037229
58

Panstruga R (2005a) Serpentine plant MLO proteins as entry portals for powdery mildew fungi. Biochem Soc Trans 33:389-392. https://doi.org/10.1042/BST0330389

10.1042/BST0330389
59

Panstruga R (2005b) Discovery of novel conserved peptide domains by ortholog comparison within plant multi-protein families. Plant Mol Biol 59:485-500. https://doi.org/10.1007/s11103-005-0353-0

10.1007/s11103-005-0353-0
60

Park S, Ahn E, Zhang D, Meinhardt LW (2025) Comparative genome-wide characterization and evolutionary insights into the AP2/ERF gene family in three Coffea species (C. canephora, C. eugenioides, and C. arabica). BMC Genomics 26:653. https://doi.org/10.1186/s12864-025-11850-0

10.1186/s12864-025-11850-040640702PMC12247349
61

Pavan S, Jacobsen E, Visser RGF, Bai Y (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed 25:1-12. https://doi.org/10.1007/s11032-009-9323-6

10.1007/s11032-009-9323-620234841PMC2837247
62

Pavan S, Schiavulli A, Appiano M, Marcotrigiano AR, Cillo F, Visser RGF, Bai Y, Lotti C, Ricciardi L (2011) Pea powdery mildew er1 resistance is associated to loss-of-function mutations at a MLO homologous locus. Theor Appl Genet 123:1425-1431. https://doi.org/10.1007/s00122-011-1677-6

10.1007/s00122-011-1677-6
63

Paysan-Lafosse T, Andreeva A, Blum M, Chuguransky SR, Grego T, Pinto BL, Salazar GA, Bileschi ML, Llinares-López F, et al. (2025) The Pfam protein families database: embracing AI/ML. Nucleic Acids Res 53:D523-D534. https://doi.org/10.1093/nar/gkae997

10.1093/nar/gkae99739540428PMC11701544
64

Reinstädler A, Müller J, Czembor JH, Piffanelli P, Panstruga R (2010) Novel induced mlo mutant alleles in combination with site-directed mutagenesis reveal functionally important domains in the heptahelical barley Mlo protein. BMC Plant Biol 10:31. https://doi.org/10.1186/1471-2229-10-31

10.1186/1471-2229-10-3120170486PMC2844067
65

Salojärvi J, Rambani A, Yu Z, Guyot R, Strickler S, Lepelley M, Wang C, Rajaraman S, Rastas P, et al. (2024) The genome and population genomics of allopolyploid Coffea arabica reveal the diversification history of modern coffee cultivars. Nat Genet 56:721-731. https://doi.org/10.1038/s41588-024-01695-w

10.1038/s41588-024-01695-w38622339PMC11018527
66

Scholes JD, Rolfe SA (1996) Photosynthesis in localised regions of oat leaves infected with crown rust (Puccinia coronata): quantitative imaging of chlorophyll fluorescence. Planta 199:573-582. https://doi.org/10.1007/BF00195189

10.1007/BF00195189
67

Shimoyama Y (2022) pyCirclize: Circular visualization in Python. https://github.com/moshi4/pyCirclize. Accessed 26 Mar 2026

68

Spinoso-Castillo JL, Corona-Torres T, Escamilla-Prado E, Morales-Ramos V, Aguilar-Rincón VH, García-de los Santos G (2021) Genetic diversity of Coffea arabica L.: a genomic approach. In: Landraces - traditional variety and natural breed. https://doi.org/10.5772/intechopen.96640

10.5772/intechopen.96640
69

Tang H, Krishnakumar V, Zeng X, Xu Z, Taranto A, Lomas JS, Zhang Y, Huang Y, Wang Y, et al. (2024) JCVI: a versatile toolkit for comparative genomics analysis. iMeta 3:e211. https://doi.org/10.1002/imt2.211

10.1002/imt2.21139135687PMC11316928
70

Thumuluri V, Almagro Armenteros JJ, Johansen AR, Nielsen H, Winther O (2022) DeepLoc 2.0: multi-label subcellular localization prediction using protein language models. Nucleic Acids Res 50:W228-W234. https://doi.org/10.1093/nar/gkac278

10.1093/nar/gkac27835489069PMC9252801
71

Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci U S A 97:11632-11637. https://doi.org/10.1073/pnas.190309197

10.1073/pnas.19030919711005831PMC17252
72

Velásquez AC, Castroverde CDM, He SY (2018) Plant–pathogen warfare under changing climate conditions. Curr Biol 28:R619-R634. https://doi.org/10.1016/j.cub.2018.03.054

10.1016/j.cub.2018.03.05429787730PMC5967643
73

Wallin E, von Heijne G (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7:1029-1038. https://doi.org/10.1002/pro.5560070420

10.1002/pro.55600704209568909PMC2143985
74

Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947-951. https://doi.org/10.1038/nbt.2969

10.1038/nbt.2969
75

Wen Z, Yao L, Wan R, Li Z, Liu C, Wang X (2015) Ectopic expression in Arabidopsis thaliana of an NB-ARC encoding putative disease resistance gene from wild Chinese Vitis pseudoreticulata enhances resistance to phytopathogenic fungi and bacteria. Front Plant Sci 6:1087. https://doi.org/10.3389/fpls.2015.01087

10.3389/fpls.2015.0108726697041PMC4674559
76

Wuthipong P, Huehne PS (2015) An analysis of cis-acting regulatory elements related to light response in the 5’ flanking region of the Ascocenda and Dendrobium actin genes. Agric Nat Resour 49:174-187

77

Zanin FC, Freitas NC, Pinto RT, Máximo WPF, Diniz LEC, Paiva LV (2022) The SAUR gene family in coffee: genome-wide identification and gene expression analysis during somatic embryogenesis. Mol Biol Rep 49:1973-1984. https://doi.org/10.1007/s11033-021-07011-7

10.1007/s11033-021-07011-7
78

Zhang Z (2022) KaKs_Calculator 3.0: calculating selective pressure on coding and non-coding sequences. Genomics Proteom Bioinform 20:536-540. https://doi.org/10.1016/j.gpb.2021.12.002

10.1016/j.gpb.2021.12.00234990803PMC9801026
79

Zheng Z, Appiano M, Pavan S, Bracuto V, Ricciardi L, Visser RGF, Wolters AMA, Bai Y (2016) Genome-wide study of the tomato SlMLO gene family and its functional characterization in response to the powdery mildew fungus Oidium neolycopersici. Front Plant Sci 7:380. https://doi.org/10.3389/fpls.2016.00380

10.3389/fpls.2016.0038027579028PMC4986958
80

Zheng Z, Nonomura T, Appiano M, Pavan S, Matsuda Y, Toyoda H, Wolters AMA, Visser RGF, Bai Y (2013) Loss of function in Mlo orthologs reduces susceptibility of pepper and tomato to powdery mildew disease caused by Leveillula taurica. PLoS One 8:e70723. https://doi.org/10.1371/journal.pone.0070723

10.1371/journal.pone.007072323923019PMC3726601
81

Zhu K, Zhao J, Lubman DM, Miller FR, Barder TJ (2005) Protein pI shifts due to posttranslational modifications in the separation and characterization of proteins. Anal Chem 77:2745-2755. https://doi.org/10.1021/ac048494w

10.1021/ac048494w
Information
  • Publisher :KOREAN SOCIETY FOR HORTICULTURAL SCIENCE
  • Publisher(Ko) :한국원예학회
  • Journal Title :Horticultural Science and Technology
  • Journal Title(Ko) :원예과학기술지
  • Received Date : 2026-08-30
  • Revised Date : 2026-09-17
  • Accepted Date : 2026-09-23
  • DOI :https://doi.org/10.7235/HORT.20260039
Journal Informaiton Horticultural Science and Technology Horticultural Science and Technology
Online Submission
  • scopus
  • NRF
  • KOFST
  • crossref crossmark
  • crossref cited-by
  • crosscheck
  • orcid
  • open access
  • ccl
Journal Informaiton Journal Informaiton - close