Attenuation of the hypersensitive response by an ATPase associated with various cellular activities (AAA) protein through suppression of a small GTPase, ADP ribosylation factor, in tobacco plants

Abstract

SummaryATPase associated with various cellular activities (AAA) proteins are commonly distributed among eukaryotes, and are involved in a multitude of cellular functions. NtAAA1 is one such example, being involved in pathogen response in tobacco plants. When its activity was suppressed in RNAi transgenic tobacco plants, an elevated resistance to the pathogenic bacterium Pseudomonas syringae was observed in comparison with the wild type. As AAA proteins function through interaction with specific partners, NtAAA1-interacting proteins were screened by the yeast two-hybrid assay, and one particular gene encoding a small GTPase, an ADP ribosylation factor, was identified and designated as NtARF. Its specific binding to NtAAA1 was confirmed by in vitro pulldown assay, and their interaction was predominant between active forms of NtARF and NtAAA1, each bound to GTP and ATP, respectively. Their physical interaction in vivo around the plasma membrane was shown by fluorescence resonance energy transfer assays, suggesting their role in membrane trafficking. Transgenic tobacco plants constitutively expressing NtARF under the control of a cauliflower mosaic virus 35S promoter exhibited spontaneous and wound-induced lesion formation, and enhanced resistance to pathogen attack. Expression of NtAAA1 in leaves of NtARF transgenic plants attenuated lesion and suppressed pathogen resistance. In wild-type tobacco plants, transcripts of NtAAA1 and NtARF could be induced by ethylene and salicylic acid, respectively. These results suggest that NtAAA1 balances plant resistance through suppression of NtARF, and that the molecular basis for the known antagonistic actions of ethylene and salicylic acid in defense response could be partly attributable to these two proteins.

Rice OsAAA-ATPase1 is Induced during Blast Infection in a Salicylic Acid-Dependent Manner, and Promotes Blast Fungus Resistance

“…Consistent with this, biochemical analysis confirmed that there was ATPase activity in the recombinant protein of OsAAA-ATPase1 ( Figure 6). Phylogenetically, OsAAA-ATPase1 was grouped within a subclade of proteins related to plant defense activation (Figure 1b), which included OsAAA-ATPase2-6 [12], tobacco NtAAA1 [18,19], and Arabidopsis AtOM66 [20]. These results suggest that OsAAA-ATPase1 belongs to the AAA-ATPase family.…”

“…AAA-type ATPases constitute a large protein family in a diverse range of organisms, and thus exhibit multiple and diverse cellular functions [15,33]. In plants, AAA-ATPase genes have been implicated in proteolysis [33], male meiosis [34], vacuolar maintenance [35], peroxisome biogenesis [36], morphogenesis [37], leaf senescence [29,38], and stress [28,39] and immune responses [18][19][20][21][22]. In this study, we present a novel rice AAA-ATPase gene member, OsAAA-ATPase1.…”

“…To assess how OsAAA-ATPase1-6 are related within the AAA-ATPase gene family, we performed a phylogenic comparison of the proteins predicted to be encoded by OsAAA-ATPase1-6 and several known rice AAA-ATPase proteins, including LMR/LRD6-6 [21,22], OsCDC48 [27], RuvBL1a [28], RLS3 [29], OsSKD1 [30], OsFtsH5 [31], and RFC5 [32], together with NtAAA1 [18,19] and AtOM66 [20]. OsAAA-ATPase1 was grouped within a subclade of proteins related to plant defense, including OsAAA-ATPase2-6, NtAAA1, and AtOM66, but, unexpectedly, distally with LMR/LRD6-6 ( Figure 1b).…”

“…Structurally, these proteins contain one or several conserved motifs, including the Walker A and Walker B motifs, which are, respectively, required for ATP binding and hydrolysis; they also contain a highly conserved amino acid sequence, referred to as the second region of homology (SRH) [16]. In plants, it has been reported that AAA-ATPase genes from Nicotiana tabacum (NtAAA1) [18,19] and Arabidopsis (AtOM66) [20] are, respectively, negatively or positively involved in the SA-signaling pathway and in the hypersensitive response (HR) upon pathogen infections. Moreover, in rice, map-based cloning of the lesion mimic resembling (lmr) mutant/lesion resembling disease (lrd6-6) mutant revealed that the corresponding gene (LMR/LRD6-6, Os06g0130000) encodes an AAA-ATPase, and is negatively involved in HR and disease resistance [21,22].…”

Tomato yellow leaf curl Sardinia virus‐resistant tomato plants expressing the multifunctional N‐terminal domain of the replication‐associated protein show transcriptional changes resembling stress‐related responses

“…No biological information is available for AT3G28510, whereas, for AATP1, one of its closest A. thaliana homologues, a role as a negative regulator of stress‐related genes has been suggested (Rama Devi et al ., ). Accordingly, the tobacco homologue NtAAA1 is involved in the attenuation of the hypersensitive response (Lee and Sano, 2007a, 2007b). We do not know the biological function of this tomato AAA‐type ATPase.…”