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The aboveground parts of terrestrial plants, collectively called the phyllosphere, have a key role in the global balance of atmospheric carbon dioxide and oxygen. The phyllosphere represents one of the most abundant habitats for microbiota colonization. Whether and how plants control phyllosphere microbiota to ensure plant health is not well understood. Here we show that the Arabidopsis quadruple mutant ( min7 fls2 efr cerk1 ; hereafter, mfec ) 1 , simultaneously defective in pattern-triggered immunity and the MIN7 vesicle-trafficking pathway, or a constitutively activated cell death1 ( cad1 ) mutant, carrying a S205F mutation in a membrane-attack-complex/perforin (MACPF)-domain protein, harbour altered endophytic phyllosphere microbiota and display leaf-tissue damage associated with dysbiosis. The Shannon diversity index and the relative abundance of Firmicutes were markedly reduced, whereas Proteobacteria were enriched in the mfec and cad1 S205F mutants, bearing cross-kingdom resemblance to some aspects of the dysbiosis that occurs in human inflammatory bowel disease. Bacterial community transplantation experiments demonstrated a causal role of a properly assembled leaf bacterial community in phyllosphere health. Pattern-triggered immune signalling, MIN7 and CAD1 are found in major land plant lineages and are probably key components of a genetic network through which terrestrial plants control the level and nurture the diversity of endophytic phyllosphere microbiota for survival and health in a microorganism-rich environment. Mutations in genes involved in immune signalling and vesicle trafficking cause defects in the leaf microbiome of Arabidopsis thaliana that result in damage to leaf tissues, suggesting mechanisms by which terrestrial plants control the level and diversity of endophytic phyllosphere microbiota.

Key Points The surface area of the phyllosphere is approximately twice as great as the land surface area, and this environment provides a habitat for numerous microorganisms that colonize leaf surfaces (where they mostly form aggregates) and the spaces inside leaves. Most phyllosphere microorganisms are bacteria, are non-pathogenic and belong to a few predominant phylogenetic groups, including the classes Alphaproteobacteria and Gammaproteobacteria and the phyla Bacteroidetes and Actinobacteria. The fungi that are also detected in the phyllosphere appear to be hyperdiverse. Numerous biotic and abiotic factors, including the plant itself, drive microbial community structure in the phyllosphere. Targeted and large-scale metaproteogenomic studies have helped to identify important mechanisms by which bacteria adapt to the phyllosphere. These mechanisms include aggregate formation, surface alterations by the production of biosurfactants, the induction of stress responses, and metabolic adaptations ranging from utilization of the C 1 compound methanol to utilization of various amino acids and sugars. The phyllosphere is a discrete habitat (or a sum of discrete habitats) and is a tractable model system for understanding the relationships between microorganisms and hosts. An improved understanding of phyllosphere microbiology is also of practical importance for biocontrol of the phyllosphere as the primary carbon-fixing unit in terrestrial systems. Compared with our understanding of the microbial ecology of the rhizosphere (the below-ground parts of plants), our understanding of the microbial ecology of the phyllosphere (the aerial parts of plants) has lagged behind, but this has begun to change in recent years. Here, Julia Vorholt reviews the latest research into the composition of microbial phyllosphere communities, the factors that drive this composition and the adaptation of these communities to the plant environment. Our knowledge of the microbiology of the phyllosphere, or the aerial parts of plants, has historically lagged behind our knowledge of the microbiology of the rhizosphere, or the below-ground habitat of plants, particularly with respect to fundamental questions such as which microorganisms are present and what they do there. In recent years, however, this has begun to change. Cultivation-independent studies have revealed that a few bacterial phyla predominate in the phyllosphere of different plants and that plant factors are involved in shaping these phyllosphere communities, which feature specific adaptations and exhibit multipartite relationships both with host plants and among community members. Insights into the underlying structural principles of indigenous microbial phyllosphere populations will help us to develop a deeper understanding of the phyllosphere microbiota and will have applications in the promotion of plant growth and plant protection.

Land plant aerial organs are covered by a hydrophobic layer called the cuticle that serves as a waterproof barrier protecting plants against desiccation, ultraviolet radiation, and pathogens. Cuticle consists of a cutin matrix as well as cuticular waxes in which very-long-chain (VLC) alkanes are the major components, representing up to 70% of the total wax content in Arabidopsis (Arabidopsis thaliana) leaves. However, despite its major involvement in cuticle formation, the alkane-forming pathway is still largely unknown. To address this deficiency, we report here the characterization of the Arabidopsis ECERIFERUM1 (CER1) gene predicted to encode an enzyme involved in alkane biosynthesis. Analysis of CER1 expression showed that CER1 is specifically expressed in the epidermis of aerial organs and coexpressed with other genes of the alkane-forming pathway. Modification of CER1 expression in transgenic plants specifically affects VLC alkane biosynthesis: waxes of TDNA insertional mutant alleles are devoid of VLC alkanes and derivatives, whereas CER1 overexpression dramatically increases the production of the odd-carbon-numbered alkanes together with a substantial accumulation of iso-branched alkanes. We also showed that CER1 expression is induced by osmotic stresses and regulated by abscisic acid. Furthermore, CER1-overexpressing plants showed reduced cuticle permeability together with reduced soil water deficit susceptibility. However, CER1 overexpression increased susceptibility to bacterial and fungal pathogens. Taken together, these results demonstrate that CER1 controls alkane biosynthesis and is highly linked to responses to biotic and abiotic stresses.

Catharanthus roseus produces a large array of terpenoid indole alkaloids (TIAs) that are an important source of natural or semisynthetic anticancer drugs. The biosynthesis of TIAs is tissue specific and induced by certain phytohormones and fungal elicitors, indicating the involvement of a complex transcriptional control network. However, the transcriptional regulation of the TIA pathway is poorly understood. Here, we describe a C. roseus WRKY transcription factor, CrWRKY1, that is preferentially expressed in roots and induced by the phytohormones jasmonate, gibberellic acid, and ethylene. The overexpression of CrWRKY1 in C. roseus hairy roots up-regulated several key TIA pathway genes, especially Tryptophan Decarboxylase (TDC), well as the transcriptional repressors ZCT1 (for zinc-finger C. roseus transcription factor 1), ZCT1, and ZCT3. However, CrWRKY1 overexpression repressed the transcriptional activators ORCA2, ORCA3, and CrMYC1. Overexpression of a dominant-repressive form of CrWRKY1, created by fusing the SRDX repressor domain to CrWRKY1, resulted in the downregulation of TDC and ZCTs but the up-regulation of ORCA3 and CrMYC2. CrWRKY1 bound to the W box elements of the TDC promoter in electrophoretic mobility shift, yeast one-hybrid, and C. roseus protoplast assays. Up-regulation of TDC increased TDC activity, tryptamine concentration, and resistance to 4-methyl tryptophan inhibition of CrWRKY1 hairy roots. Compared with control roots, CrWRKY1 hairy roots accumulated up to 3-fold higher levels of serpentine. The preferential expression of CrWRKY1 in roots and its interaction with transcription factors including ORCA3, CrMYC2, and ZCTs may play a key role in determining the root-specific accumulation of serpentine in C. roseus plants.

The phytohormone auxin regulates nearly all aspects of plant growth and development. Tremendous achievements have been made in elucidating the tryptophan (Trp)-dependent auxin biosynthetic pathway; however, the genetic evidence, key components, and functions of the Trp-independent pathway remain elusive. Here we report that the Arabidopsis indole synthase mutant is defective in the long-anticipated Trp-independent auxin biosynthetic pathway and that auxin synthesized through this spatially and temporally regulated pathway contributes significantly to the establishment of the apical–basal axis, which profoundly affects the early embryogenesis in Arabidopsis . These discoveries pave an avenue for elucidating the Trp-independent auxin biosynthetic pathway and its functions in regulating plant growth and development. Significance The phytohormone indole-3-acetic acid (IAA) plays a vital role in plant growth and development. IAA can be synthesized through the precursor tryptophan (Trp), known as the Trp-dependent IAA biosynthetic pathway. However, IAA may also be synthesized through a proposed Trp-independent IAA biosynthetic pathway. Although the Trp-independent IAA biosynthesis was hypothesized 20 years ago, it remains a mystery. In this paper, we provide compelling evidence that the cytosol-localized indole synthase (INS) initiates the Trp-independent IAA biosynthetic pathway and that the spatial and temporal expression of INS plays an important role in the establishment of the apical–basal pattern during early embryogenesis, demonstrating that the Trp-dependent and -independent IAA biosynthetic pathways coordinately regulate embryogenesis of higher plants.

BackgroundThe optimal defence hypothesis (ODH) predicts that tissues that contribute most to a plant's fitness and have the highest probability of being attacked will be the parts best defended against biotic threats, including herbivores. In general, young sink tissues and reproductive structures show stronger induced defence responses after attack from pathogens and herbivores and contain higher basal levels of specialized defensive metabolites than other plant parts. However, the underlying physiological mechanisms responsible for these developmentally regulated defence patterns remain unknown.ScopeThis review summarizes current knowledge about optimal defence patterns in above- and below-ground plant tissues, including information on basal and induced defence metabolite accumulation, defensive structures and their regulation by jasmonic acid (JA). Physiological regulations underlying developmental differences of tissues with contrasting defence patterns are highlighted, with a special focus on the role of classical plant growth hormones, including auxins, cytokinins, gibberellins and brassinosteroids, and their interactions with the JA pathway. By synthesizing recent findings about the dual roles of these growth hormones in plant development and defence responses, this review aims to provide a framework for new discoveries on the molecular basis of patterns predicted by the ODH.ConclusionsAlmost four decades after its formulation, we are just beginning to understand the underlying molecular mechanisms responsible for the patterns of defence allocation predicted by the ODH. A requirement for future advances will be to understand how developmental and defence processes are integrated.

The ARP2/3 complex, a highly conserved nucleator of F-actin, and its activator, the SCAR complex, are essential for growth in plants and animals. In this article, we present a pathway through which roots of Arabidopsis thaliana directly perceive light to promote their elongation. The ARP2/3-SCAR complex and the maintenance of longitudinally aligned F-actin arrays are crucial components of this pathway. The involvement of the ARP2/3-SCAR complex in light-regulated root growth is supported by our finding that mutants of the SCAR complex subunit BRK1/HSPC300, or other individual subunits of the ARP2/3-SCAR complex, showed a dramatic inhibition of root elongation in the light, which mirrored reduced growth of wildtype roots in the dark. SCAR1 degradation in dark-grown wild-type roots by constitutive photomorphogenic 1 (COP1) E3 ligase and 26S proteasome accompanied the loss of longitudinal F-actin and reduced root growth. Light perceived by the root photoreceptors, cryptochrome and phytochrome, suppressed COP1-mediated SCAR1 degradation. Taken together, our data provide a biochemical explanation for light-induced promotion of root elongation by the ARP2/3-SCAR complex.

Environmental stress causes membrane damage in plants. Lipid studies are required to understand the adaptation of plants to climate change. Here, LC-MS-based lipidomic and microarray transcriptome analyses were carried out to elucidate the effect of short-term heat stress on the Arabidopsis thaliana leaf membrane. Vegetative plants were subjected to high temperatures for one day and then grown under normal conditions. Sixty-six detected glycerolipid species were classified according to patterns of compositional change by Spearman’s correlation coefficient. Triacylglycerols, 36:4- and 36:5-monogalactosyldiacylglycerol, 34:2- and 36:2-digalactosyldiacylglycerol, 34:1-, 36:1- and 36:6-phosphatidylcholine and 34:1-phosphatidylethanolamine increased by the stress and immediately decreased during recovery. The relative amount of one triacylglycerol species (54:9) containing α-linolenic acid (18:3) increased under heat stress. These results suggest that heat stress in Arabidopsis leaves induces an increase in triacylglycerol levels, which functions as an intermediate of lipid turnover and results in a decrease in membrane polyunsaturated fatty acids. Microarray data revealed candidate genes responsible for the observed metabolic changes.

A CBL-interacting protein kinase (CIPK) gene, BnCIPK6, was isolated in Brassica napus. Through yeast two-hybrid screening, 27 interaction partners (including BnCBL1) of BnCIPK6 were identified in Brassica napus. Interaction of BnCIPK6 and BnCBL1 was further confirmed by BiFC (bimolecular fluorescence complementation) in plant cells. Expressions of BnCIPK6 and BnCBL1 were significantly up-regulated by salt and osmotic stresses, phosphorous starvation, and abscisic acid (ABA). Furthermore, BnCIPK6 promoter activity was intensively induced in cotyledons and roots under NaCl, mannitol, and ABA treatments. Transgenic Arabidopsis plants with over-expressing BnCIPK6, its activated form BnCIPK6M, and BnCBL1 enhanced high salinity and low phosphate tolerance, suggesting that the functional interaction of BnCBL1 and BnCIPK6 may be important for the high salinity and phosphorous deficiency signalling pathways. In addition, activation of BnCIPK6 confers Arabidopsis plants hypersensitive to ABA. On the other hand, over-expression of BnCIPK6 in Arabidopsis cipk6 mutant completely rescued the low-phosphate-sensitive and ABA-insensitive phenotypes of this mutant, further suggesting that BnCIPK6 is involved in the plant response to high-salinity, phosphorous deficiency, and ABA signalling.

In plants, phosphoglycerate kinase (PGK) converts 1,3-bisphosphoglycerate into 3-phosphoglycerate in glycolysis but also participates in the reverse reaction in gluconeogenesis and the Calvin-Benson cycle. In the databases, we found three genes that encode putative PGKs. Arabidopsis (Arabidopsis thaliana) PGK1 was localized exclusively in the chloroplasts of photosynthetic tissues, while PGK2 was expressed in the chloroplast/plastid of photosynthetic and nonphotosynthetic cells. PGK3 was expressed ubiquitously in the cytosol of all studied cell types. Measurements of carbohydrate content and photosynthetic activities in PGK mutants and silenced lines corroborated that PGK1 was the photosynthetic isoform, while PGK2 and PGK3 were the plastidial and cytosolic glycolytic isoforms, respectively. The pgk1.1 knockdown mutant displayed reduced growth, lower photosynthetic capacity, and starch content. The pgk3.2 knockout mutant was characterized by reduced growth but higher starch levels than the wild type. The pgk1.1 pgk3.2 double mutant was bigger than pgk3.2 and displayed an intermediate phenotype between the two single mutants in all measured biochemical and physiological parameters. Expression studies in PGK mutants showed that PGK1 and PGK3 were down-regulated in pgk3.2 and pgk1.1, respectively. These results indicate that the down-regulation of photosynthetic activity could be a plant strategy when glycolysis is impaired to achieve metabolic adjustment and optimize growth. The double mutants of PGK3 and the triose-phosphate transporter (pgk3.2 tpt3) displayed a drastic growth phenotype, but they were viable. This implies that other enzymes or nonspecific chloroplast transporters could provide 3-phosphoglycerate to the cytosol. Our results highlight both the complexity and the plasticity of the plant primary metabolic network.