Development of fusarium wilt resistant mutants of Musa spp. cv.Rasthali (AAB, Silk subgroup) and comparative proteomic analysis along with its wild type.
Banana cv. Rasthali
EMS
Fusaric acid
Fusarium wilt resistance
LD50
Journal
Planta
ISSN: 1432-2048
Titre abrégé: Planta
Pays: Germany
ID NLM: 1250576
Informations de publication
Date de publication:
05 Mar 2022
05 Mar 2022
Historique:
received:
17
09
2021
accepted:
16
02
2022
entrez:
6
3
2022
pubmed:
7
3
2022
medline:
9
3
2022
Statut:
epublish
Résumé
Induced mutagenesis using embryogenic cell suspension (ECS) explants with toxin based screening is an effective tool to create non-chimeral Fusarium wilt resistant mutants in banana. Global proteomics unravel the molecular mechanism behind resistance. Race 1 of Fusarium wilt is a serious threat to Musa spp. cv.Rasthali (AAB, Silk subgroup) which is a choice variety traditionally grown in most of the south East Asian countries. Resistant gene introgression into susceptible varieties through conventional breeding has several limitations and the predominant ones being sterility and long generation time. Under such circumstances, induced mutagenesis combined with toxin based in vitro screening remains as the viable alternative for the development of fusarium wilt resistant Rasthali. Therefore, induced mutagenesis was attempted by using ethylmethane sulfonate (EMS) in embryogenic cell suspension (ECS) of Rasthali followed by in vitro screening for fusarium wilt resistance using new generation toxins and pot screening through challenge inoculation with Foc race 1. This ultimately resulted in the identification of 15 resistant lines. Global proteomic analysis in one of the resistant mutant lines namely NRCBRM15 and its wild type revealed 37 proteins, of which 20 showed differential expression. Out of 20 proteins, nineteen were significantly abundant in NRCBRM15 and only one was abundant in wild Rasthali. A total of nine genes based on protein expression were further validated using quantitative real time polymerase chain reaction (qRT-PCR). Annotation results revealed that some of the genes namely Enolase, ATP synthase-alpha subunit, Actin 2, Actin 3,-glucanase, UTP-glucose-1-phosphate uridylyltransferase, Respiratory burst oxidase homolog, V type proton ATPase catalytic subunit A and DUF292 domain containing protein are involved in diverse functions such as carbohydrate metabolism, energy production, electron carrier, response to wounding, binding proteins, cytoskeleton organization, extracellular region, structural molecule and defense.
Identifiants
pubmed: 35249170
doi: 10.1007/s00425-022-03860-z
pii: 10.1007/s00425-022-03860-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
80Subventions
Organisme : Bhabha Atomic Research Centre
ID : 35/14/46/BRNS-2014
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Bancroft J (1876) Report of the board appointed to enquire into the cause of disease affecting livestock and plants. Votes Proc 3:1011–1038
Barrero RA, Umeda M, Yamamura S, Uchimiya H (2002) Arabidopsis CAP regulates the actin cytoskeleton necessary for plant cell elongation and division. Plant Cell 14:149–163
pubmed: 11826305
pmcid: 150557
Bhagwat B, Duncan EJ (1998) Mutation breeding of Highgate (Musa acuminata, AAA) for tolerance to Fusarium oxysporum f. sp. cubense using gamma irradiation. Euphytica 101(2):143–150
Bidabadi SS, Jain SM (2020) Cellular, molecular, and physiological aspects of in vitro plant regeneration. Plants 9(6):702
Broertjes C (1977) Artificially induced genetic variation in fruit trees. Acta Hortic 75:19–26
Broertjes C, Leffring L (1972) Mutation breeding of Kalanchoe. Euphytica 21(3):415–423
Buddenhagen CE, Chimera C, Clifford P (2009) Assessing biofuel crop invasiveness: a case study. PLoS ONE 4(4):5261
Carlier J, De Wale D, Escalant JV (2002) Global evaluation of Musa germplasm for resistance to Fusarium wilt, Mycosphaerella leaf spot diseases and nematodes (Technical guidelines No. 6). INIBAP, Montpellier, p 57
Carvalhais LC, Henderson J, Rincon-Florez VA, O’Dwyer C, Czislowski E, Aitken EA, Drenth A (2019) Molecular diagnostics of banana Fusarium Wilt targeting secreted-in-xylem genes. Front Plant Sci 31(10):547
Chen WQ, Swart WJ (2002) The in vitro phytotoxicity of culture filtrates of Fusarium oxysporum to five genotypes of Amaranthus hybridus. Euphytica 127(1):61–67
Chen L, Zhong HY, Kuang JF, Li JG, Lu WJ, Chen JY (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234(2):377–390
pubmed: 21505864
pmcid: 21505864
Chen L, Xiang S, Chen Y, Li D, Yu D (2017) Arabidopsis WRKY45 interacts with the DELLA protein RGL1 to positively regulate age-triggered leaf senescence. Mole Plant 10(9):1174–1189
Chittarath K, So T, Sor S, Rungsawang W, Pongsapich P, Kong G, Thomas JE, Geering AD (2017) First record of papaya ringspot virus in Cambodia and confirmation of its presence in Laos. Australas Plant Dis Notes 12(1):1–2
Chittoor JM, Leach JE, White FF (1997) Differential induction of a peroxidase gene family during infection of rice by Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 10(7):861–871
pubmed: 9304860
Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014) Identification of a plant receptor for extracellular ATP. Science 343(6168):290–294
pubmed: 24436418
Christelová P, De Langhe E, Hřibová E et al (2017) Molecular and cytological characterization of the global Musa germplasm collection provides insights into the treasure of banana diversity. Biodivers Conserv 26:801–824
Crino P (1997) Culture filtrate as selective agent of resistance to phytopathogenic fungi. In: Upadhyay RK, Mukerji KG (eds) Toxins in plant disease development and evolving biotechnology. Science Publishers, Enfield, pp 183–208
Cvikrova M, Binarova P, Eder J, Nedělník J (1992) Accumulation of phenolic acids in filtrate-treated alfalfa cell cultures derived from genotypes with different susceptibility to Fusarium oxysporum. J Plant Physiol 140(1):21–27
Dhed’a DB, Dumortier F, Panis B, Vuylsteke D (1991) Plant regeneration in cell suspension cultures of the cooking banana cv. Bluggoes’ (Musa spp. ABB group). Fruits 46:125–135
Dita M, Barquero M, Heck D, Mizubuti ES, Staver CP (2018) Fusarium wilt of banana: current knowledge on epidemiology and research needs toward sustainable disease management. Front Plant Sci 9:1468
pubmed: 30405651
pmcid: 6202804
Dixon RA, Harrison MJ, Lamb CJ (1994) Early events in the activation of plant defense responses. Ann Rev Phytopathol 32:479–501
Escalant JV, Teisson C, Cote F (1994) Amplified somatic embryogenesis from male flowers of triploid banana and plantain cultivars (Musa spp.). Vitro Plant 30(4):181–186
Facchini PJ, Penzes C, Johnson AG, Bull D (1996) Molecular characterization of berberine bridge enzyme genes from opium poppy. Plant Physiol 112(4):1669–1677
pubmed: 8972604
pmcid: 158100
FAO/IAEA (2006) Towards the establishment of a TILLING platform for Musa. Plant Breeding Unit - Activities Report. pp 7–11
Food and Agriculture Organizations of United Nations (2019) Banana market review. http://www.fao.org . Accessed 13 Mar 2020
Gentile V, Thomazy V, Piacentini M, Fesus L, Davies PJ (1992) Expression of tissue transglutaminase in Balb-C 3T3 fibroblasts: effects on cellular morphology and adhesion. J Cell Biol 119(2):463–474
pubmed: 1356992
Gert HJK, André D, Miguel D, Kees J, Sietze V, Jetse JS (2021) Editorial: Fusarium Wilt of banana, a recurring threat to global banana production. Front Plant Sci 11:2177
Ghag SB (2019) Fusarium wilt disease of banana in India: current scenario. Agrotech (editorial) 8:121
Henty-Ridilla JL, Li J, Day B, Staiger CJ (2014) Actin depolymerising factor 4 regulates actin dynamics during innate immune signalling in Arabidopsis. Plant Cell 26(1):340–352
pubmed: 24464292
pmcid: 3963580
Hohmann U, Jacobs G, Jung C (2005) An EMS mutagenesis protocol for sugar beet and isolation of non-bolting mutants. Plant Breed 124:317–321
Jain SM (2010) Mutagenesis in crop improvement under the climate change. Rom Biotechnol Lett 15(2):88–106
Jankowicz Cieslak J, Huynh OA, Brozynska M et al (2012) Induction, rapid fixation and retention of mutations in vegetatively propagated banana. Plant Biotechnol J 10(9):1056–1066
pubmed: 22928630
pmcid: 3533788
Jeter CR, Tang W, Henaff E, Butterfield T, Roux SJ (2004) Evidence of a novel cell signalling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis. Plant Cell 16(10):2652–2664
pubmed: 15367717
pmcid: 520962
Jiménez-Quesada MJ, Traverso JÁ, Alché JD (2016) NADPH oxidase-dependent superoxide production in plant reproductive tissues. Front Plant Sci 7:359
pubmed: 27066025
pmcid: 4815025
Karve A, Rauh BL, Xia X, Kandasamy M, Meagher RB, Sheen J, Moore BD (2008) Expression and evolutionary features of the hexokinase gene family in Arabidopsis. Planta 228(3):411–425
pubmed: 18481082
pmcid: 2953952
Kobayashi Y, Kobayashi I (2013) Micro-wounding is a pivotal factor for the induction of actin-dependent penetration resistance against fungal attack. Planta 237:1187–1198
pubmed: 23328898
Koo AJ, Gao X, Daniel Jones A, Howe GA (2019) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59(6):974–986
Kumaravel M, Uma S, Backiyarani S, Saraswathi MS, Vaganan MM, Muthusamy M, Sajith KP (2017) Differential proteome analysis during early somatic embryogenesis in Musa spp. AAA cv. Grand Naine. Plant Cell Rep 36(1):163–178
pubmed: 27807644
Kuźniak E, Patykowski J, Urbanek H (1999) Involvement of the antioxidative system in tomato response to fusaric acid treatment. J Phytopathol 147(7–8):385–390
Laemmli U (1970) Most commonly used discontinuous buffer system for SDS electrophoresis. Nature 227:680–686
pubmed: 5432063
Lee TM, Su SF, Chou TF, Lee YT, Tsai CH (2002) Loss of preconditioning by attenuated activation of myocardial ATP-sensitive potassium channels in elderly patients undergoing coronary angioplasty. Circulation 105(3):334–340
pubmed: 11804989
Li C, Shao J, Wang Y, Li W, Guo D, Yan B, Xia Y, Peng M (2013) Analysis of banana transcriptome and global gene expression profiles in banana roots in response to infection by race 1 and tropical race 4 of Fusarium oxysporum f. sp. cubense. BMC Genom 14(1):1–6
Li J, Henty-Ridilla JL, Staiger BH, Day B, Staiger CJ (2015) Capping protein integrates multiple MAMP signalling pathways to modulate actin dynamics during plant innate immunity. Nat Commun 28:7206
Luhua S, Ciftci-Yilmaz S, Harper J, Cushman J, Mittler R (2008) Enhanced tolerance to oxidative stress in transgenic Arabidopsis plants expressing proteins of unknown function. Plant Physiol 148(1):280–292
pubmed: 18614705
pmcid: 2528079
Marina N, Teschemacher AG, Kasparov S, Gourine AV (2016) Glia, sympathetic activity and cardiovascular disease. Exp Physiol 101(5):565–576
pubmed: 26988631
pmcid: 5031202
Matsumoto K, Barbosa ML, Souza LAC (1995) Race 1 Fusarium wilt tolerance on banana plants selected by fusaric acid. Euphytica 84:67
Matsumoto K, Barbosa ML, Souza LAC, Teixeira JB (2010) In vitro selection for resistance to Fusarium wilt in banana. Mass screening techniques for selecting crops resistant to disease, vol 6. IAEA, Vienna, pp 101–113
Mba C, Afza R, Shu QY (2012) Mutagenic radiations: X-rays, ionizing particles and ultraviolet. In: Forster BP, Nakagawa H, Shu QY (eds) Plant mutation breeding and biotechnology. CABI, Wallingford, pp 83–90
Mendicino J (1960) Sucrose phosphate synthesis in wheat germ and green leaves. J Biol Chem 235(12):3347–3352
pubmed: 13769376
Morpurgo R, Lopato SV, Afza R, Novak FJ (1994) Selection parameters for resistance to Fusarium oxysporum f. sp. cubense race 1 and race 4 on diploid banana (Musa acuminata Colla). Euphytica 75:121–129
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assay with tobacco tissue culture. Physiol Plant 15:473–497
Musoke C, Rubaihayo PR, Magambo M (1999) Gamma rays and ethyl-ethane sulphonate in vitro induced Fusarium wilt resistant mutants in bananas. Afr Crop Sci J 7(4):313–320
Natarajan S, Xu C, Caperna TJ, Garrett WM (2005) Comparison of protein solubilization methods suitable for proteomic analysis of soybean seed proteins. Ann Biochem 343:214e20
Nedelnik J, Repkova J (1998) Plant selection in vitro for resistance to some pathogens using secondary toxic metabolites. Genetika a Slechteni UZPI (czech Republic) 34(2):69–76
Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9(6):255–262
pubmed: 2466658
Novak FJ, Brunner H, Afza R, Morpurgo R, Upadhyay RK, Van Duren M, Sacchi M, Hawz JS, Khatri A, Kahl G, Kaemmer D, Ramser J, Weising K (1993) Improvement of Musa through biotechnology and mutation breeding. In: Biotechnology applications for banana and plantain improvement, proceedings of the workshop, international network for the improvement of banana and plantain (INIBAP), pp 143–158
Omar MS, Novak FJ, Brunner H (1989) In vitro action of ethyl ethane sulphonate on banana shoots tips. Sci Hortic 40:283–295
Owji H, Hajiebrahimi A, Seradj H, Hemmati S (2017) Identification and functional prediction of stress responsive AP2/ERF transcription factors in Brassica napus by genome-wide analysis. Comput Biol Chem 71:32–56
pubmed: 28961511
País SM, Téllez-Iñón MT, Capiati DA (2009) Serine/threonine protein phosphatases type 2A and their roles in stress signalling. Plant Signal Behav 4(11):1013–1015
pubmed: 20009558
pmcid: 2819506
Park CJ, Seo YS (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 31(4):32
Parwinder K, Ricarda J, Krishnapillai S, Martin JB (2011) Proteome analysis of the Albugo candida-Brassica juncea pathosystem reveals that the timing of the expression of defense-related genes is a crucial determinant of pathogenesis. J Exp Bot 62:1285e98
Percipalle P (2013) Co-transcriptional nuclear actin dynamics. Nucleus 4:43–52
pubmed: 23138849
pmcid: 3585027
Péros JP, Chagvardieff P (1987) Toxic effect of Ustilago scitaminea on sugarcane callus. II. Culture filtrate action and comparison with the effects of U. maydis and kinetin/Toxischer Effekt von Ustilago scitaminea auf Zuckerrohr-Kallus. II. Wirkung von Kulturfiltrat und Vergleich mit dem Einfluß von U. maydis und Kinetin. Zeitschrift Für Pflanzenkrankheiten Und Pflanzenschutz J Plant Dis Prot 1:301–307
Ploetz RC, Vazquez A, Haynes JL (1999) Response of new banana accessions in South Florida to Panama disease. Crop Prot 18(7):445–449
Porter K, Day B (2016) From filaments to function: the role of the plant actin cytoskeleton in pathogen perception, signalling and immunity. J Integr Plant Biol 58(4):299–311
pubmed: 26514830
Porter K, Shimono M, Tian M, Day B (2012) Arabidopsis actin-depolymerizing factor-4 links pathogen perception, defense activation and transcription to cytoskeletal dynamics. PLoS Pathog 8:e1003006
pubmed: 23144618
pmcid: 3493479
Predieri S, Di Virgilio N (2007) In vitro mutagenesis and mutant multiplication. In: Jain SM, Haggman H (eds) Protocols for micropropagation of woody trees and fruits. Springer, pp 323–333
Raz V, Fluhr R (1993) Ethylene signal is transduced via protein phosphorylation events in plants. Plant Cell 5(5):523–530
pubmed: 12271074
pmcid: 160290
Remotti PC, Löffler HJM (1996) The involvement of fusaric acid in the bulb-rot of Gladiolus. Phytopathol 144:405–411
Ribeiro LR, Oliveira SASD, Amorim EP, Serejo JAS, Haddad F (2018) Sources of resistance to Fusarium oxysporum f. sp. cubense in banana germplasm. Rev Bras Frutic 40(1):e-202
Riker AJ, Riker RS (1936) Introduction to research on plant diseases. St Louis, Chicago, p 117
Robertson AS, Smythe E, Ayscough KR (2009) Functions of actin in endocytosis. Cell Mol Life Sci 66:2049–2065
pubmed: 19290477
Rojas B, Rautiala P, Mappes J (2014) Differential detectability of polymorphic warning signals under varying light environments. Behav Process 109:164–172
Roux N (2004) Mutation induction in Musa—review. In: Jain SM, Swennen R (eds) Banana improvement: cellular molecular biology and induced mutations. Science Publishers Inc, Enfield, pp 23–32
Roux P, Gauthier-Rouvière C, Doucet-Brutin S, Fort P (1997) The small GTPases Cdc42Hs, Rac1 and RhoG delineate Raf-independent pathways that cooperate to transform NIH3T3 cells. Curr Biol 7(9):629–637
pubmed: 9285711
Roux N, Dolezel J, Swennen R, Zapata-Arias FJ (2001) Effectiveness of three micropropagation techniques to dissociate cytochimeras in Musa spp. Plant Cell Tiss Org 66(3):189–197
Russo-Marie F (1992) Macrophages and the glucocorticoids. J Neuroimmunol 40(2–3):281–286
pubmed: 1430158
Sabine (2019) Banana Fusarium Wilt Tropical Race 4: a mounting threat to global banana markets? The recent spread and potential future impact of the disease on global banana trade. In: Commodity Focus. FAO Food Outlook, pp 15–20
Saindrenan P, Barchietto T, Bompeix G (1990) Effects of phosphonate on the elicitor activity of culture filtrates of Phytophthora cryptogea in Vigna unguiculata. Plant Sci 67:245–251
Saraswathi MS, Kannan G, Uma S, Thangavelu R, Backiyarani S (2016) Improvement of banana cv. Rasthali (Silk, AAB) against Fusarium oxysporum f.sp. cubense (VCG 0124/5) through induced mutagenesis: determination of LD50 specific to mutagen, explants, toxins and in vitro and in vivo screening for Fusarium wilt resistance. Indian J Exp Biol 54:345–353
pubmed: 27319054
Savin VN, Swaminathan MS, Sharma B (1968) Enhancement of chemically-induced mutation frequency in barley through alteration in the duration of pre-soaking of seeds. Mutat Res 6:101–107
Schoofs H, Panis B, Strosse H, Mayo Mosqueda A, Lopez Torres J, Roux N, Dolezel J, Swennen R (1999) Bottlenecks in the generation and maintenance of morphogenic banana cell suspensions and plant regeneration via somatic embryogenesis there from. Info Musa 18(2):3–7
Schoofs H, Panis B, Swennen R (1997) Competence of scalps for somatic embryogenesis in Musa. In: I International symposium on banana in the subtropics, Puerto La Cruz, Spain, Acta Hortic (1998) 490, pp 475–484
Sharifi G, Ebrahimzadeh H, Ghareyazie B, Gharechahi J, Vatankhah E (2012) Identification of differentially accumulated proteins associated with embryogenic and non-embryogenic calli in saffron (Crocus sativus L.). Proteome Sci 10(1):1–5
Sigurbjörnsson B (1977) Introduction: mutations in plant breeding programs, manual on mutation breeding second edition technical report series, vol 119. IAEA, pp 1–6
Song C, Hu KN, Joo CG, Swager TM, Griffin RG (2006) Totapol: a biradical polarizing agent for dynamic nuclear polarization experiments in aqueous media. J Am Chem Soc 128(35):11385–11390
pubmed: 16939261
Strosse H, R Domergue, B Panis, JV Escalant, F Côte (2003) Banana and plantain embryogenic cell suspensions. In: Vézina A, Picq C (eds). INIBAP Technical Guidelines 8. The International Network for the Improvement of Banana and Plantain, Montpellier, France, p 36
Supriya S (2019) Mechanism of ATPase. News-Medical, viewed 29 March 2021. https://www.news-medical.net/life-sciences/Mechanism-of-ATPase.aspx . Accessed Mar 2021
Svabova L, Lebeda A (2005) In vitro selection for improved plant resistance to pathogens. J Phytopathol 153:52–64
Tanaka S, Han X, Kahmann R (2015) Microbial effectors target multiple steps in the salicylic acid production and signalling pathway. Front Plant Sci 6:349
pubmed: 26042138
pmcid: 4436567
Thangavelu R, Gopi M (2015) Field suppression of Fusarium wilt disease in banana by the combined application of native endophytic and rhizospheric bacterial isolates possessing multiple functions. Phytopathol Mediterr 54:241–252
Thangavelu R, Mustaffa MM (2010) First report on the occurrence of a virulent strain of Fusarium wilt pathogen (Race-1) infecting Cavendish (AAA) group of bananas in India. Plant Dis 94:1379
pubmed: 30743652
Thangavelu R, Muthukathan G, Pushpakanth P, Murugan L, Raj EE, Marimuthu N, Prabakaran M, Uma S (2020) First report of Fusarium oxysporum f.sp. cubense VCG 0125 and VCG 01220 of Race 1 infecting Cavendish bananas (Musa sp. AAA) in India. Plant Dis 5:45. https://doi.org/10.1094/PDIS-09-20-2052-PDN
doi: 10.1094/PDIS-09-20-2052-PDN
Thangavelu R, Saraswathi MS, Uma S, Loganathan M, Backiyarani S, Durai P, Raj EE, Marimuthu N, Kannan G, Swennen R (2021) Identification of sources resistant to a virulent Fusarium wilt strain (VCG 0124) infecting Cavendish bananas. Sci Rep 11(1):1–4
Tian M, Chaudhry F, Ruzicka DR, Meagher RB, Staiger CJ, Day B (2009) Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB. Plant Physiol 150:815–824
pubmed: 19346440
pmcid: 2689984
Tripathi D, Zhang T, Koo AJ, Stacey G, Tanaka K (2018) Extracellular ATP acts on jasmonate signalling to reinforce plant defense. Plant Physiol 176(1):511–523
pubmed: 29180381
Van Harten AM (1998) Mutation breeding. Cambridge University Press, Cambridge, p 353. https://doi.org/10.1017/S0021859699257073
doi: 10.1017/S0021859699257073
Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141(2):384–390
pubmed: 16760492
pmcid: 1475453
Van Duren M, Morpurgo R, Dolezel J, Afza R (1996) Induction and verification of auto tetraploids in diploid banana (Musa acuminata) by in vitro techniques. Euphytica 88(1):25–34
Van den Bulk RW (1991) Application of cell and tissue culture and in vitro selection for disease resistance breeding—a review. Euphytica 56(3):269–285
Venkatesh N, Keller NP (2019) Mycotoxins in conversation with bacteria and fungi. Front Microbiol 10:403
pubmed: 30941105
pmcid: 6433837
Vuylsteke D, Schoofs J, Swennen R, Adejare G, Ayodele M, De Langhe E (1990) Shoot-tip culture and third-country quarantine to facilitate the introduction of new Musa germplasm into West Africa. Plant Genet Resour Newsl 81(82):5–11
Weerasinghe AJ, Schmiesing C, Sinn E (2009) Highly sensitive and selective reversible sensor for the detection of Cr
Wu YL, Yi GJ, Peng XX (2010) Rapid screening of Musa species for resistance to Fusarium wilt in an in vitro bioassay. Eur J Plant Pathol 128(3):409–415
Xiao RF, Zhu YJ, Li YD, Liu B (2013) Studies on vascular infection of Fusarium oxysporum f. sp. cubense race 4 in banana by field survey and green fluorescent protein reporter. Sci J Plant Pathol 2:44–51
Yong J, Bischof H, Burgstaller S, Siirin M, Murphy A, Malli R, Kaufman RJ (2019) Mitochondria supply ATP to the ER through a mechanism antagonized by cytosolic Ca
Zhang Y, Ficarro SB, Li S, Marto JA (2009) Optimized Orbitrap HCD for quantitative analysis of phosphopeptides. J Am Soc Mass Spectrom 20(8):1425–1434
pubmed: 19403316
Zheng SJ, García-Bastidas FA, Li X, Zeng L, Bai T, Xu S, Yin K, Li H, Fu G, Yu Y, Yang L (2018) New geographical insights of the latest expansion of Fusarium oxysporum f. sp. cubense tropical race 4 into the greater Mekong sub region. Front Plant Sci 9:457
pubmed: 29686692
pmcid: 5900031
Zhou LJ, Zhang CL, Zhang RF, Wang GL, Li YY, Hao YJ (2019) The SUMO E3 ligase MdSIZ1 targets MdbHLH104 to regulate plasma membrane H+-ATPase activity and iron homeostasis. Plant Physiol 179(1):88–106
pubmed: 30333149