ALD1 accumulation in Arabidopsis epidermal plastids confers local and non-autonomous disease resistance.

The Arabidopsis plastid-localized ALD1 protein acts in the lysine catabolic pathway that produces infection-induced pipecolic acid (Pip), Pip derivatives, and basal non-Pip metabolite(s). ALD1 is indispensable for disease resistance associated with Pseudomonas syringae infections of naïve plants as well as those previously immunized by a local infection, a phenomenon called systemic acquired resistance (SAR). Pseudomonas syringae is known to associate with mesophyll as well as epidermal cells. To probe the importance of epidermal cells in conferring bacterial disease resistance, we studied plants in which ALD1 was only detectable in the epidermal cells of specific leaves. Local disease resistance and many features of SAR were restored when ALD1 preferentially accumulated in the epidermal plastids at immunization sites. Interestingly, SAR restoration occurred without appreciable accumulation of Pip or known Pip derivatives in secondary distal leaves. Our findings establish that ALD1 has a non-autonomous effect on pathogen growth and defense activation. We propose that ALD1 is sufficient in the epidermis of the immunized leaves to activate SAR, but basal ALD1 and possibly a non-Pip metabolite(s) are also needed at all infection sites to fully suppress bacterial growth. Thus, epidermal plastids that contain ALD1 play a key role in local and whole-plant immune signaling.

Glucose-Regulated HLP1 Acts as a Key Molecule in Governing Thermomemory.

Induction of heat shock proteins (HSPs) in response to heat stress (HS) is indispensable for conferring thermotolerance. Glc, a fundamental signaling and metabolic molecule, provides energy to stressed seedlings to combat stress. The recovery of stressed plants from detrimental HS in response to Glc is largely mediated by HSPs, but the mechanistic basis of this thermotolerance is not well defined. In this study, we show that Glc has a prominent role in providing thermotolerance. Glc-mediated thermotolerance involves HSP induction via the TARGET OF RAPAMYCIN (TOR)-E2Fa signaling module. Apart from HSPs, TOR-E2Fa also regulates the Arabidopsis (Arabidopsis thaliana) ortholog of human Hikeshi, named HIKESHI-LIKE PROTEIN1 (HLP1). Expression of proHLP1::GUS in the shoot apical meristem (SAM) after HS coincides with TOR-E2Fa expression, substantiating a role for TOR-E2Fa-HLP1 in providing thermotolerance. We also demonstrate that Glc along with heat could induce proliferation activity in the SAM after HS recovery, which was arrested by the TOR inhibitor AZD-8055. Molecular and physiological studies suggest that HS-activated heat stress transcription factor A1s also positively regulate HLP1 transcription, suggesting convergence of the Glc and HS signaling pathways. Loss of functional HLP1 causes HS hypersensitivity, whereas HLP1 overexpressors display increased thermotolerance. HLP1 binds to the promoters of Glc-regulated HS-responsive genes and promotes chromatin acetylation. In addition, Glc modifies the chromatin landscape at thermomemory-related loci by promoting H3K4 trimethylation (H3K4me3). Glc-primed accumulation of H3K4me3 at thermomemory-associated loci is mediated through HLP1. These findings reveal the novel function of Glc-regulated HLP1 in mediating thermotolerance/thermomemory response.

Over-expression of Arabidopsis thaliana SFD1/GLY1, the gene encoding plastid localized glycerol-3-phosphate dehydrogenase, increases plastidic lipid content in transgenic rice plants.

Lipids are the major constituents of all membranous structures in plants. Plants possess two pathways for lipid biosynthesis: the prokaryotic pathway (i.e., plastidic pathway) and the eukaryotic pathway (i.e., endoplasmic-reticulum (ER) pathway). Whereas some plants synthesize galactolipids from diacylglycerol assembled in the plastid, others, including rice, derive their galactolipids from diacylglycerols assembled by the eukaryotic pathway. Arabidopsis thaliana glycerol-3-phosphate dehydrogenase (G3pDH), coded by SUPPRESSOR OF FATTY ACID DESATURASE 1 (SFD1; alias GLY1) gene, catalyzes the formation of glycerol 3-phosphate (G3p), the backbone of many membrane lipids. Here SFD1 was introduced to rice as a transgene. Arabidopsis SFD1 localizes in rice plastids and its over-expression increases plastidic membrane lipid content in transgenic rice plants without any major impact on ER lipids. The results suggest that over-expression of plastidic G3pDH enhances biosynthesis of plastid-localized lipids in rice. Lipid composition in the transgenic plants is consistent with increased phosphatidylglycerol synthesis in the plastid and increased galactolipid synthesis from diacylglycerol produced via the ER pathway. The transgenic plants show a higher photosynthetic assimilation rate, suggesting a possible application of this finding in crop improvement.

Arabidopsis thaliana GLUTATHIONE-S-TRANSFERASE THETA 2 interacts with RSI1/FLD to activate systemic acquired resistance.

A partly infected plant develops systemic acquired resistance (SAR) and shows heightened resistance during subsequent infections. The infected parts generate certain mobile signals that travel to the distal tissues and help to activate SAR. SAR is associated with epigenetic modifications of several defence-related genes. However, the mechanisms by which mobile signals contribute to epigenetic changes are little known. Previously, we have shown that the Arabidopsis REDUCED SYSTEMIC IMMUNITY 1 (RSI1, alias FLOWERING LOCUS D; FLD), which codes for a putative histone demethylase, is required for the activation of SAR. Here, we report the identification of GLUTATHIONE-S-TRANSFERASE THETA 2 (GSTT2) as an interacting factor of FLD. GSTT2 expression increases in pathogen-inoculated as well as pathogen-free distal tissues. The loss-of-function mutant of GSTT2 is compromised for SAR, but activates normal local resistance. Complementation lines of GSTT2 support its role in SAR activation. The distal tissues of gstt2 mutant plants accumulate significantly less salicylic acid (SA) and express a reduced level of the SA biosynthetic gene PAL1. In agreement with the established histone modification activity of FLD, gstt2 mutant plants accumulate an enhanced level of methylated and acetylated histones in the promoters of WRKY6 and WRKY29 genes. Together, these results demonstrate that GSTT2 is an interactor of FLD, which is required for SAR and SAR-associated epigenetic modifications.

Exogenous application of histone demethylase inhibitor trans-2-phenylcyclopropylamine mimics FLD loss-of-function phenotype in terms of systemic acquired resistance in Arabidopsis thaliana.

Plants often learn from previous infections to mount higher level of resistance during subsequent infections, a phenomenon referred to as systemic acquired resistance (SAR). During primary infection, mobile signals generated at the infection site subsequently move to the rest of plant to activate SAR. SAR activation is associated with alteration in the nucleosomal composition at the promoters of several defense-related genes. However, genetic regulations of such epigenetic modifications are largely obscure. Recently, we have demonstrated that Reduced Systemic immunity1/FLOWERING LOCUS D (RSI1; alias FLD) a homolog of human histone demethylase, is required for SAR development in Arabidopsis. Here, we report that exogenous application of a histone demethylase inhibitor trans-2-phenylcyclopropylamine (2-PCPA) mimics rsi1/fld loss-of-function phenotypes in terms of SAR and associated histone demethylation at the promoters of PR1, WRKY 29, and WRKY6 genes, and as well as flowering phenotypes. Our results suggest histone demethylase activity of FLD is important for controlling SAR activation.