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Physiological Changes in Barley Mlo-11 Powdery Mildew Resistance Conditioned by Tandem Repeat Copy Number

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Physiological Changes in Barley Mlo-11 Powdery Mildew Resistance Conditioned by Tandem Repeat Copy Number International Journal of Molecular Sciences Article Physiological Changes in Barley mlo-11 Powdery Mildew Resistance Conditioned by Tandem Repeat Copy Number Cynthia Ge 1, Paula Moolhuijzen 1 , Lee Hickey 2 , Elzette Wentzel 1, Weiwei Deng 1, Eric G. Dinglasan 2 and Simon R. Ellwood 1,* 1 Centre for Crop and Disease Management, School of Molecular and Life Sciences, Curtin University, Bentley, WA 6102, Australia; [email protected] (C.G.); [email protected] (P.M.); [email protected] (E.W.); [email protected] (W.D.) 2 Centre Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St. Lucia, QLD 4069, Australia; [email protected] (L.H.); [email protected] (E.G.D.) * Correspondence: [email protected] Received: 28 October 2020; Accepted: 17 November 2020; Published: 20 November 2020 Abstract: Wild barley accessions have evolved broad-spectrum defence against barley powdery mildew through recessive mlo mutations. However, the mlo defence response is associated with deleterious phenotypes with a cost to yield and fertility, with implications for natural fitness and agricultural productivity. This research elucidates the mechanism behind a novel mlo allele, designated mlo-11(cnv2), which has a milder phenotype compared to standard mlo-11. Bisulphite sequencing and histone ChIP-seq analyses using near-isogenic lines showed pronounced repression of the Mlo promoter in standard mlo-11 compared to mlo-11(cnv2), with repression governed by 24 nt heterochromatic small interfering RNAs. The mlo-11(cnv2) allele appears to largely reduce the physiological effects of mlo while still endorsing a high level of powdery mildew resistance. RNA sequencing showed that this is achieved through only partly restricted expression of Mlo, allowing adequate temporal induction of defence genes during infection and expression close to wild-type Mlo levels in the absence of infection. The two mlo-11 alleles showed copy number proportionate oxidase and peroxidase expression levels during infection, but lower amino acid and aromatic compound biosynthesis compared to the null allele mlo-5. Examination of highly expressed genes revealed a common WRKY W-box binding motif (consensus ACCCGGGACTAAAGG) and a transcription factor more highly expressed in mlo-11 resistance. In conclusion, mlo-11(cnv2) appears to significantly mitigate the trade-off between mlo defence and normal gene expression. Keywords: Hordeum vulgare; Blumeria graminis f. sp. hordei; gene silencing; histone modification; reactive oxygen species (ROS) 1. Introduction Barley is an important cereal crop globally, ranked fourth in terms of total quantity produced (http://www.fao.org/in-action/inpho/crop-compendium/cereals-grains/en/). Powdery mildews are obligate biotrophic fungal diseases which in barley are caused by Blumeria graminis f. sp. hordei (Bgh). The fungus stunts barley growth, reduces yield, and can downgrade grain quality from malting to animal feed. Broad-spectrum resistance to powdery mildew that confers resistance to all races of Bgh is determined by recessive mutations of the Mlo gene. Mlo is an enigmatic and broadly conserved plant gene with mlo-governed resistance reported in both monocot and dicot species (reviewed in [1]). In barley, over 30 artificially induced mlo alleles are known to exist [2]. The gene is responsive to Int. J. Mol. Sci. 2020, 21, 8769; doi:10.3390/ijms21228769 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 18 death [3,4]. mlo alleles act via rapid formation of large cell-wall appositions (CWA) and necrosis that correlate with resistance in epidermal cells. The CWA phenotype is also observed in nonhost resistance to powdery mildew, for example, following inoculation of barley with wheat powdery mildew [5]. Int. J. Mol. Sci. 2020, 21, 8769 2 of 18 A natural form of barley mlo resistance, known as mlo-11, involves a wild-type Mlo gene that is silenced via an upstreambiotic and abiotic tandem stimuli, isrepeat involved array in developmental consisting processes, of the and isMlo a negative 5′ UTR regulator and of cellexons 1–5 [6]. Both induced mutantsdeath and [3 ,4the]. mlo originalalleles act viaor rapid standard formation mlo-11 of large cell-wall exhibit appositions undesirable (CWA) and side necrosis effects, that with necrotic correlate with resistance in epidermal cells. The CWA phenotype is also observed in nonhost resistance leaf spotting, chlorosis,to powdery and mildew, leaf for example,senescence following (Fig inoculationure 1). of barleyBreeders with wheat have powdery overcome mildew [5]. these effects, with most European springA natural cultivars form of now barley mlocontainingresistance, known mlo resistance as mlo-11, involves [7,8]. a wild-type Ge et Mloal. [9]gene uncovered that a second is silenced via an upstream tandem repeat array consisting of the Mlo 50 UTR and exons 1–5 [6]. natural variant ofBoth mlo-11 induced mutantswith andan theapparently original or standard fewermlo-11 pleiotropicexhibit undesirable effects, side eff ects,named with necrotic mlo-11(cnv2), which showed partial resistanceleaf spotting, chlorosis, to powdery and leaf senescence mildew (Figure in 1s).eedling Breeders have leaves overcome and these full e ffects, resistance with most in adult leaves. European spring cultivars now containing mlo resistance [7,8]. Ge et al. [9] uncovered a second natural The variant had variantjust two of mlo-11 copieswith anof apparently the tandem fewer pleiotropic repeat earray,ffects, named comparedmlo-11(cnv2 to), which 11–12 showed in standard mlo-11, and lacked spontaneouspartial resistance cell to powderydeath mildewin uninfected in seedling leaves leaves and full and resistance death in adult of leaves. underlying The variant mesophyll cells had just two copies of the tandem repeat array, compared to 11–12 in standard mlo-11, and lacked during infection,spontaneous characteristic cell death inof uninfected mlo alleles leaves and with death ofa underlyingstronger mesophyll effect. cells Other during infection,partial mlo resistance phenotypes, conferredcharacteristic by of missensemlo alleles with mutati a strongerons, effect. have Other partialbeenmlo reportedresistance phenotypes, in barley conferred (mlo-12 by and mlo-28 [3]) missense mutations, have been reported in barley (mlo-12 and mlo-28 [3]) and a series of alleles provide and a series of allelesvarying provide levels of potency varying in wheat levels [10]. of potency in wheat [10]. Figure 1. Field-grownFigure 1.barleyField-grown Pallas barley 22 Pallas (mlo-5 22 ()mlo-5 plants) plants displaying displaying chlorosis chlorosis and senescence and senescence on the on the right- right-hand side, compared to a wild-type Mlo line Pallas 18 on the left-hand side. hand side, compared to a wild-type Mlo line Pallas 18 on the left-hand side. The mlo-11(cnv2) phenotype appears to correspond to the relative Mlo expression level differences compared to standard mlo-11 [9], and, on the basis of DNA methylation sequencing, the authors The mlo-11(postulatedcnv2) phenotype that this may involve appears small RNA-directed to correspond DNA methylation to the (RdDM). relative DNA methylation Mlo expression level differences comparedwas first to discovered standard in plants, mlo-11 and research [9], hasand, consequently on the demonstratedbasis of DNA an elaborate methylation role in plant sequencing, the development and environmental responses through histone modifications [11,12]. Previous studies authors postulatedrevealed that silencing this ofmay transposable involve elements small and repetitive RNA-directed heterochromatic DNA sequences methylation by RdDM [13] (RdDM). DNA methylation wasand first histone discovered H3K9 methylation in plants, [14], while and repression research of regions has consequently and genes in euchromatic demonstrated regions an elaborate occurs via H3K27 methylation [15]. H3K4 methylation, associated with actively transcribed genes, role in plant developmentoccurs in euchromatic and regions. environmental In addition to methylation, responses acetylation through of histones histone leads to remodelling modifications [11,12]. Previous studiesof condensedrevealed chromatin, silencing leading toof gene transposable activation [16]. elements and repetitive heterochromatic The precise functions and molecular basis of mlo resistance remain little understood, although a sequences by RdDMrole in immunity[13] and or histone suppression H3K9 of defence methylat responses ision implicit [14], with while the wild-type repression gene negatively of regions and genes in euchromatic regulatingregions plantoccurs defence via responses, H3K27 with methylation similar sets of co-expressed [15]. H3K4 genes demonstrated methylation, in both associated with Arabidopsis and barley [4,17,18]. Aside from measurable yield and phenotypic effects associated with actively transcribedmlo alleles, genes, resource occurs requirements in euchromatic of this resistance re andgions. defence In against addition pathogens to inmethylation, general have acetylation of histones leads tobeen remodelling a matter of some of conjecture.condensed A trade-o chffromatin,between energy leading for growth to gene and activation activation of defence [16]. The precise functions and molecular basis of mlo resistance remain little understood, although a role in immunity or suppression of defence responses is implicit with the wild-type gene negatively regulating plant defence responses, with
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