Nuclear processes associated with plant immunity and pathogen susceptibility

Briefings in Functional Genomics, 14(4), 2015, 243–252 doi: 10.1093/bfgp/elv013 Advance Access Publication Date: 6 April 2015 Review paper Nuclear processes associated with plant immunity and pathogen susceptibility Corresponding author. Edgar Huitema, Senior Lecturer, Division of Plant Sciences, College of Life Sciences, University of Dundee, Errol Road, Invergowrie, DD2 5DA Dundee. Tel.: +44 (0)1382 568921; Fax: 01382 568575; E-mail: *These authors contributed equally to this work. Abstract Plants are sessile organisms that have evolved exquisite and sophisticated mechanisms to adapt to their biotic and abiotic environment. Plants deploy receptors and vast signalling networks to detect, transmit and respond to a given biotic threat by inducing properly dosed defence responses. Genetic analyses and, more recently, next-generation -omics approaches have allowed unprecedented insights into the mechanisms that drive immunity. Similarly, functional genomics and the emergence of pathogen genomes have allowed reciprocal studies on the mechanisms governing pathogen virulence and host susceptibility, collectively allowing more comprehensive views on the processes that govern disease and resistance. Among others, the identification of secreted pathogen molecules (effectors) that modify immunity-associated processes has changed the plant–microbe interactions conceptual landscape. Effectors are now considered both important factors facilitating disease and novel probes, suited to study immunity in plants. In this review, we will describe the various mechanisms and processes that take place in the nucleus and help regulate immune responses in plants. Based on the premise that any process required for immunity could be targeted by pathogen effectors, we highlight and describe a number of functional assays that should help determine effector functions and their impact on immune-related processes. The identification of new effector functions that modify nuclear processes will help dissect nuclear signalling further and assist us in our bid to bolster immunity in crop plants. Key words: nucleus; immunity; pathogen; effector; susceptibility; next-generation sequencing (NGS) Graham B. Motion is a PhD student in the Huitema Laboratory at the University of Dundee. His research is focused on the identification of Phytophthora effectors, which target and directly bind host DNA. This is being carried out by creating an algorithm to computationally predict DNA binding effectors, which can then be confirmed and characterized using wet-lab techniques. Tiago M.M.M. Amaro is a PhD student in the Huitema Laboratory at the University of Dundee. His research focuses on the roles of nuclear effectors from Phytophthora capsici towards virulence. He is also interested in connecting the activities of nuclear effectors to changes in the post-translational status of the host nuclear proteome. Natalja Kulagina is a PhD student in the Huitema Laboratory at the University of Dundee. Her research is focused on Phytophthora capsici nuclear effectors and their function. She is interested in the identification of core components in terms of effector–host interaction, and targeting such components with synthetic biology to enhance immunity. Edgar Huitema is a senior lecturer in the Division of Plant Sciences, College of Life Sciences at the University of Dundee. The Huitema Laboratory studies the biology of secreted pathogen proteins (effectors) from Phytophthora capsici that accumulate in the host nucleus and compromise the plant immune system during infection. The overall aim of this research is to bolster the plant immune system in important dicot crops and perturb infection-associated processes in a bid to limit the dramatic losses caused by Phytophthora spp. C The Author 2015. Published by Oxford University Press. V This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 243 Graham B. Motion*, Tiago M.M.M. Amaro*, Natalja Kulagina and Edgar Huitema 244 | Motion et al. Introduction Nuclear processes that drive immunity and may be targeted by pathogens Nuclear transport Translocation of immune regulatory and signalling proteins into the nucleus marks the onset of the host nucleus’ involvement in the immunity process. Nuclear trafficking is mediated by importins, exportins and nucleoporins, all of which are involved in transport of cargo across the nuclear envelope [9]. Proteins representing diverse functions are transported into the nucleus and include classes of transcriptional regulators, which form a complex network and direct plant immune responses through transcriptional reprogramming [11]. Interestingly, an increasing number of Resistance (R) proteins such as Resistance to Ralstonia solanacearum 1 (RRS1), N, Mildew Locus A (MLA), resistance to Pseudomonas syringae 4 (RPS4), RX require nuclear transport for activation (reviewed in [12]). Tomato RPS4 recognizes Pseudomonas syringae AvrRps4 resulting in nuclear accumulation of the plant immune regulator EDS1 [13], while barley MLA was shown to be directly associated with several transcription factors (TFs), essential for plant defences (WRKY, MYB6) [14]. These findings indicate the crucial role of nuclear trafficking in plant immune signalling. Given the importance of plant nuclear dynamics for plant immunity, it is not surprising that its components are targeted, imitated or required by pathogens to promote infection. In Nicotiana benthamiana, Xanthomonas campestris pv. vesicatoria AvrBs3 effector was shown to contain a Nuclear Localisation Signal (NLS) and mimic eukaryotic TFs, affecting host cell development [15]. Effector activity can also modify the subcellular localization of their corresponding target proteins. The Phytophthora infestans effector Pi03192 (PITG_03192) targets two NAC [NAM (no apical meristem), ATAF, CUC (cup-shaped cotyledon)] TFs, thereby preventing NAC relocalization to the nucleus during infection and after PTI stimulation [16]. Furthermore, Arabidopsis thaliana nucleo-trafficking proteins of the Modifier of SNC1 (MOS) family were reported to be involved in plant basal and constitutive resistance [17]. For instance, Agrobacterium tumefasciens NLS-containing effectors VirD2 and VirE2 can interact with several importins to translocate bacterial T-DNA into the host nucleus [18, 19]. In the meantime, silencing of Importin a 1 or 2 in N. benthamiana was shown to negatively affect the nuclear import of several P. infestans effectors [20], suggesting requirement of host machinery by the pathogen. These findings illustrate the critical role nucleo-cytoplasmic transport plays in immunity and how pathogens either co-opt or modify these processes to their benefit. Plants are continuously challenged by biot (...truncated)