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Effector Identification in the Lettuce Downy Mildew Bremia Lactucae By bs_bs_banner MOLECULAR PLANT PATHOLOGY (2012) 13(7), 719–731 DOI: 10.1111/J.1364-3703.2011.00780.X Effector identification in the lettuce downy mildew Bremia lactucae by massively parallel transcriptome sequencing JOOST H. M. STASSEN1, MICHAEL F. SEIDL2,3, PIM W. J. VERGEER1, ISAÄC J. NIJMAN4, BEREND SNEL2,3, EDWIN CUPPEN4 AND GUIDO VAN DEN ACKERVEKEN1,3,* 1Plant–Microbe Interactions, Department of Biology, Utrecht University, Padualaan 8, 3508 CH Utrecht, the Netherlands 2Theoretical Biology and Bioinformatics, Department of Biology, Utrecht University, Padualaan 8, 3508 CH Utrecht, the Netherlands 3Centre for BioSystems Genomics (CBSG), Wageningen University, Binnenhaven 5, 6709 PD Wageningen, the Netherlands 4Hubrecht Institute, Developmental Biology and Stem Cell Research, KNAW and University Medical Center Utrecht, Uppsalalaan 8, Utrecht, the Netherlands agent of the Irish potato famine, and P. ramorum, which causes SUMMARY sudden oak death. The downy mildews have a narrow host range, Lettuce downy mildew (Bremia lactucae) is a rapidly adapting for instance Hyaloperonospora arabidopsidis grows only on living oomycete pathogen affecting commercial lettuce cultivation. Arabidopsis thaliana plants, Plasmopara viticola is an important Oomycetes are known to use a diverse arsenal of secreted proteins grape pathogen and Bremia lactucae is the most important patho- (effectors) to manipulate their hosts. Two classes of effector are gen of lettuce (Lactuca sativa). The control of B. lactucae is an known to be translocated by the host: the RXLRs and Crinklers. To increasingly difficult task as fungicides have been phased out gain insight into the repertoire of effectors used by B. lactucae to because of environmental concerns, and fungicide resistance is manipulate its host, we performed massively parallel sequencing becoming more widespread (Brown et al., 2004). Genetically con- of cDNA derived from B. lactucae spores and infected lettuce trolled resistance to B. lactucae is present in most commercial (Lactuca sativa) seedlings. From over 2.3 million 454 GS FLX reads, lettuce varieties, but is quickly overcome by new rapidly evolving 59 618 contigs were assembled representing both plant and B. lactucae races. pathogen transcripts. Of these, 19 663 contigs were determined to The B. lactucae life cycle starts from a spore landing on the be of B. lactucae origin as they matched pathogen genome plant’s epidermis, followed by penetration, hyphal colonization of sequences (SOLiD) that were obtained from >270 million reads of host tissue and sporulation, leading to the release of large spore-derived genomic DNA. After correction of cDNA sequencing numbers of spores. At all stages, B. lactucae is in contact with its errors with SOLiD data, translation into protein models and filter- host, so that it can interfere with defence and manipulate host ing, 16 372 protein models remained, 1023 of which were pre- processes to obtain nutrients. In contrast with many oomycetes, dicted to be secreted. This secretome included elicitins, necrosis B. lactucae infection usually starts with the direct germination and ethylene-inducing peptide 1-like proteins, glucanase inhibi- of asexual spores, without a zoospore intermediate stage. tors and lectins, and was enriched in cysteine-rich proteins. Can- B. lactucae also does not rely on entry via stomata, but, instead, didate host-translocated effectors included 78 protein models usually penetrates directly through the cuticula into an epidermal with RXLR effector features. In addition, we found indications for cell. A primary vesicle and, later, a secondary vesicle are then an unknown number of Crinkler-like sequences. Similarity cluster- formed in the epidermal cell, after which hyphae grow in the ing of secreted proteins revealed additional effector candidates. intercellular space of the mesophyll tissue. Haustoria are formed in We provide a first look at the transcriptome of B. lactucae and its most mesophyll and epidermal cells encountered by the hyphae encoded effector arsenal. (reviewed in Lebeda et al., 2008). The B. lactucae–lettuce interac- tion is a classic example of a gene-for-gene interaction, in which single dominant avirulence genes in B. lactucae are genetically recognized by dominant resistance genes in lettuce (reviewed by Michelmore and Wong, 2008). Knowledge on the molecular INTRODUCTION biology and basis of B. lactucae pathogenicity, however, is mostly Oomycete plant pathogens cause devastating diseases on a wide lacking. variety of crops. These organisms resemble fungi, but are more Studies of oomycete–plant interactions at the molecular level closely related to brown algae. Well-known oomycete pathogens are now revealing more and more details on the molecular toolbox are the obligate biotrophic downy mildews and the hemibio- used by these remarkable pathogens. The genomes of the trophic Phytophthora species, including P. infestans, the causative sequenced oomycete species Albugo candida (Kemen et al., 2011), A. laibachii (Links et al., 2011), H. arabidopsidis (Baxter *Correspondence: Email: [email protected] et al., 2010), P. infestans (Haas et al., 2009), P. sojae (Tyler et al., © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD 719 720 J. H. M. STASSEN et al. 2006), P. ramorum (Tyler et al., 2006) Pseudoperonospora cuben- 2009; Tian et al., 2007) and suppression of effector-triggered sis (Tian et al., 2011) and Pythium ultimum (Lévesque et al., immunity (e.g. Kelley et al., 2010; Liu et al., 2011). In addition, the 2010) represent a treasure trove of information on the effector first cytoplasmic target and mode of action of a host-translocated repertoires secreted by these pathogens to manipulate their effector has been identified; host E3 ligase CMPG1 is stabilized by hosts. Various types of effectors are predicted to act in the apo- P. infestans effector AVR3a (Bos et al., 2010), revealing more plast and, in addition, two classes of oomycete effector translo- details about the mechanisms by which oomycetes establish a cate into the host cell (reviewed in Stassen and Van den successful infection of their hosts. Ackerveken, 2011). Effectors from one of the host-translocated In this article, we investigate the potential effector arsenal of classes are referred to as RXLR effectors, after the RXLR amino B. lactucae by cDNA sequencing and de novo assembly of tran- acid motif contained by the first characterized effectors of this script sequences. Transcripts obtained from B. lactucae-infected class (Rehmany et al., 2005), although variations in this motif lettuce were compared with short reads of B. lactucae genomic also permit host translocation (Kale et al., 2010). Examples of DNA (gDNA) to select for B. lactucae transcripts. From the variants of RXLR motifs include the QXLR motif found in host- predicted B. lactucae secretome, we identified homologues of translocating effectors of the oomycete pathogen of cucumber, known effector families as well as new groups of potential effector Ps. cubensis (Tian et al., 2011), and the GXLR motif found in the proteins. P. infestans effector SNE1 (Kelley et al., 2010). Furthermore, ATR5 of H. arabidopsidis is recognized inside host cells and has RESULTS homology to the RXLR motif-containing effectors, but does not contain an RXLR motif (Bailey et al., 2011). A second class of Bremia lactucae transcriptome sequencing host-translocated effectors are the Crinklers, which contain two conserved amino acid motifs preceding a modular C-terminal Two sources of RNA were used for B. lactucae transcriptome section. In a number of Crinklers, the domains that form the sequencing: RNA isolated from asexual B. lactucae conidiospores modules in this C-terminal section induce cell death when and RNA isolated from B. lactucae-infected lettuce leaves. Many expressed in Nicotiana benthamiana (Haas et al., 2009). Two effector genes are known to be differentially expressed during Crinklers from P. sojae are even thought to be indispensable for different stages of infection, with transcripts of early-stage effec- successful infection of soybean (Liu et al., 2011). Although the tors being present in spores, and transcripts of later stage (hyphal effector repertoire is generally highly divergent between species, growth) effectors being expressed in B. lactucae growing features such as motifs associated with host-translocated effec- in planta.To increase the number of different infection stages and, tors allow for the identification of potential effectors encoded by as a result, transcript diversity, lettuce seedlings were inoculated gene models or mRNA sequences. twice with a 3-day interval (see time line in Fig. 1A). Lettuce Access to the catalogue of the effectors of a species allows for seedlings were inoculated with conidiospores (Fig. 1B) that ger- the cloning and investigation of individual effector genes. This has minate on the leaf surface, penetrate through epidermal cells and led to the identification of various activities of effectors on host then continue to grow intercellular hyphae in the mesophyll, processes. Examples include the disruption of host cell wall– forming haustoria in plant cells (Fig. 1C). Plants were kept under membrane adhesion (Bouwmeester et al., 2011), suppression of low relative humidity and, as a result, when material was har- defensive protease activity (Kaschani et al., 2010; Song et al., vested for RNA isolation (day 7), no B. lactucae sporulation was (A) Fig. 1 Preparation of Bremia lactucae-infected
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