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Downy Mildew in Lettuce

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Post time 2021-12-7 12:01:02 | Show all posts |Read mode
(Contributed by Li Bo)

        Cultivated lettuce (Lactuca sativa L.)is susceptible to downy mildew disease caused by the biotrophic oomycete Bremialactucae Regel. This pathogen can infect lettuce plants at anydevelopmental stages, causing yellow to pale-green lesions that eventuallybecome necrotic[1].      
        Simkoet al.[2] determined that Batavia type cultivar 'LaBrillante' has a high level of field resistance to the disease in California. Testing of a mapping population developed from a crossbetween 'Salinas 88' and La Brillante in multiple field and laboratoryexperiments revealed that at least five loci conferred resistance in LaBrillante. The presence of a new dominant resistance gene (designated Dm50)that confers complete resistance to specific isolates was detected inlaboratory tests of seedlings inoculated with multiple diverse isolates. Dm50is located in the major resistance cluster on linkage group 2 that contains atleast eight major, dominant Dm genes conferring resistance to downymildew. A quantitative trait locus (QTL) located at the Dm50 chromosomalregion (qDM2.2) was detected, when the amount of disease was evaluated a monthbefore plants reached harvest maturity. Four additional QTL for resistance to B.lactucae were identified on linkage groups 4 (qDM4.1 and qDM4.2), 7(qDM7.1), and 9 (qDM9.2). The largest effect was associated with qDM7.1 (up to32.9% of the total phenotypic variance) that determined resistance in multiplefield experiments.
       Plant-pathogenicoomycetes secrete effector proteins to suppress host immune responses.Resistance proteins may recognize effectors and activate immunity, which isoften associated with a hypersensitive response (HR)[3]. Transientexpression of effectors in plant germplasm and screening for HR has proven tobe a powerful tool in the identification of new resistance genes[4,5,6,7,8]. Pelgromet al.[9] screened14 effectors from the lettuce downy mildew Bremia lactucae race Bl:24for HR induction in over 150 lettuce accessions. Three effectors—BLN06, BLR38and BLR40—were recognized in specific lettuce lines. The recognition ofeffector BLR38 in Lactuca serriola LS102 did not co-segregate withresistance against race Bl:24, but was linked to resistance against multipleother B. lactucae races. Two unlinked loci are both required foreffector recognition and are located near known major resistance clusters. Genedosage affects the intensity of the BLR38- triggered HR, but is of minorimportance for disease resistance.
Meisrimleret al.[10] reportthe discovery of an effector-target hub consisting of four B. lactucae effectorsand one lettuce protein target. Interaction of the lettuce tail-anchored NACtranscription factor, LsNAC069, with B. lactucae effectors does notrequire the Nterminal NAC domain but depends on the C-terminal region includingthe transmembrane domain. In Y2H experiments, B. lactucae effectorsinteract with Arabidopsis and potato tail-anchored NACs, suggesting that theyare conserved effector targets. Transient expression of RxLR effector proteinsBLR05 and BLR09 and their target LsNAC069 in planta revealed a predominantlocalization to the endoplasmic reticulum. Phytophthora capsici culturefiltrate and polyethylene glycol treatment induced relocalization to thenucleus of a stabilized LsNAC069 protein, lacking the NAC-domain (LsNAC069ΔNAC).Relocalization was significantly reduced in the presence of theSer/Cys-protease inhibitor TPCK indicating proteolytic cleavage of LsNAC069allows for relocalization. LsNAC069 silenced lettuce lines had decreasedLsNAC069 transcript levels but did not show significantly alteredsusceptibility to B. lactucae. In contrast, LsNAC069 silencingincreased resistance to Pseudomonas cichorii bacteria and reduced wiltingeffects under moderate drought stress, indicating a broad role of LsNAC069 inabiotic and biotic stress responses.
       Pelgromet al.[11] used a lettuce cDNAlibrary-based yeast two-hybrid system, 61 protein-protein interactions wereidentified, involving 21 B. lactucae effectors and 46 unique lettuceproteins. The top ten interactors based on the number of independent coloniesidentified in the Y2H and two interactors that belong to gene families involvedin plant immunity, were further characterized. This study determined thesubcellular localization of the fluorescently tagged lettuce proteins and theirinteracting effectors. Importantly, relocalization of effectors or theirinteractors to the nucleus was observed for four proteinpairs upon theirco-expression, supporting their interaction in planta.
       Parraet al.[12] used two RILs, originating fromcrosses between the field resistant cultivars Grand Rapids and Iceberg andsusceptible cultivars Salinas and PI491224, were evaluated for downy mildewresistance under field conditions. In all, 160 RILs from the Iceberg × PI491224and 88 RILs from the Grand Rapids × Salinas populations were genotyped usinggenotyping by sequencing, which generated 906 and 746 high-quality markers,respectively, that were used for quantitative trait locus (QTL) analysis. Theyfound a QTL in chromosome 4 that is present in both Grand Rapids × Salinas andIceberg × PI491224 populations that has a major effect on field resistance.They also found two additional significant QTLs in chromosomes 2 and 5 in the Iceberg× PI491224 RIL population.  
       Parraet al.[13] used low-pass,whole genome sequencing of 11 NILs to identify the chromosome segmentsintrogressed from the wild donor species, mapped an additional 11 Dmgenes to diferent positions in the L. sativa cv. Salinas referencegenome, six of them to genomic intervals no larger than 6 Mb.

Reference:
[1] Wu BM, van Bruggen AH, Subbarao KV,Pennings GG. Spatial analysis of lettuce 438 downy mildew using geostatics andgeographic information systems. Phytopathology. 2001, 439 91(2):134-142.
[2] Simko I, Ochoa OE, Pel MA, Tsuchida C,Font I Forcada C, Hayes RJ, Truco MJ, Antonise R, Galeano CH, Michelmore RW.Resistance to Downy Mildew in Lettuce 'La Brillante'is Conferred by Dm50 Gene and Multiple QTL. Phytopathology. 2015, 105(9):1220-8.
[3 ] Jones, J.D.G. and Dangl, J.L. Theplant immune system. Nature. 2006, 444, 323–329.
[4]Giesbers, A.K.J., Pelgrom, A.J.E., Visser, R.G.F., Niks, R.E., Van denAckerveken, G. and Jeuken, M.J.W. Effector-mediated discovery of a novelresistance gene against Bremia lactucae in a nonhost lettuce species. NewPhytol. 2017, 216, 915–926.
[5]Stassen, J.H., Boer, E.D., Vergeer, P.W., Andel, A., Ellendorff, U., Pelgrom,K., Pel, M., Schut, J., Zonneveld, O., Jeuken, M.J. and Van den Ackerveken, G.Specific in planta recognition of two GKLR proteins of the downy mildewBremia lactucae revealed in a large effector screen in lettuce. Mol.Plant–Microbe Interact. 2013, 26, 1259–1270
[6]Vleeshouwers, V.G.A.A. and Oliver, R.P. Effectors as tools in diseaseresistance breeding against biotrophic, hemibiotrophic, and necrotrophic plantpathogens. Mol. Plant–Microbe Interact. 2014, 27, 196–206.
[7]Vleeshouwers, V.G., Rietman, H., Krenek, P., Champouret, N., Young, C., Oh,S.K., Wang, M., Bouwmeester, K., Vosman, B., Visser, R.G. and Jacobsen, E. Effectorgenomics accelerates discovery and functional profiling of potato disease resistanceand Phytophthora Infestans avirulence genes. PLoS One, 2008, 3, e2875.
[8]Wroblewski, T., Caldwell, K.S, Piskurewicz, U., Cavanaugh, K.A, Xu, H., Kozik,A., Ochoa, O., McHale, L.K, Lahre, K., Jelenska, J., Castillo, J.A, Blumenthal,D., Vinatzer, B.A, Greenberg, J.T and Michelmore, R.W. Comparative large-scaleanalysis of interactions between several crop species and the effectorrepertoires from multiple pathovars of Pseudomonas and Ralstonia. PlantPhysiol.2009, 150, 1733–1749
[9]Pelgrom AJE, Eikelhof J, Elberse J, Meisrimler CN, Raedts R, Klein J, Van denAckerveken G. Recognitionof lettuce downy mildew effector BLR38 in Lactuca serriolaLS102 requires two unlinked loci. Mol Plant Pathol. 2019, 20(2):240-253.
[10] Meisrimler CN, Pelgrom AJE, Oud B,Out S, Van den Ackerveken G. Multiple downy mildew effectors target thestress-related NAC transcription factor LsNAC069 in lettuce. Plant J. 2019, 99(6):1098-1115.
[11] Pelgrom AJE, Meisrimler CN, ElberseJ, Koorman T, Boxem M, Van den Ackerveken G. Host interactors of effector proteins ofthe lettuce downy mildew Bremia lactucae obtained by yeasttwo-hybrid screening. PLoS One. 2020, 15(5):e0226540
[12]Parra L, Simko I, Michelmore RW. Identification of Major Quantitative TraitLoci Controlling Field Resistance to Downy Mildew in Cultivated Lettuce( Lactuca sativa). Phytopathology, 2021, 111(3):541-547.
[13]Parra L, Nortman K, Sah A, Truco MJ, Ochoa O, Michelmore R. Identification andmapping of new genes for resistanceto downy mildew in lettuce.Theor Appl Genet. 2021, 134(2):519-528.

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