Holo-omic applications to unveil microbiome shaping sustainable horticultural production

Plant-associated microorganisms play a key role in the future sustainability of terrestrial ecosystems. In nature, plants and their associated microbiome can form an assemblage of species, considered interacting metaorganisms or holobionts. Horticultural plants, including vegetables, fruit and berries, and ornamentals live in intimate association with complex and diverse microbial communities that have evolved a myriad of cooperative and competitive interaction mechanisms that shape the holobiont fitness. Nonetheless, our understanding of these interactions in shaping more complex microbial horticulture communities, along with their relevance for host growth, fitness, stress resilience, and health in a more natural context remains sparse. In this perspective, the holo-omic landscape that requires careful consideration of study design and integrates multi-omic data from both host and microbiota domains is a promising approach to unveil the interplay between the two to advance horticultural production. The analysis of horticulture (meta)-omics and phenotyping, along with mechanistic experiments in model systems, is revolutionizing research by enhancing our ability to understand the structure and core function of the plant-associated microbiome. These advancements are complemented by improvements in the throughput and accuracy of DNA sequencing, enabling us to delve deeper into the genomes of microbial communities. Yet, many challenges remain. We focus this review on the potential for holo-omics to generate a more holistic perspective of molecular networks, and we further discuss the implementation and current limitations of the holo-omic approach within microbial horticulture. We argue that holo-omics will pave the way to improve, from a horticultural perspective, food security and safety, sustainability, breeding practices, development of microbiota- and host-tailored horticultural crops’ health treatments and increasing production efficiency

Plant-microbiome interactions under drought—insights from the molecular machinist’s toolbox

Plants face numerous challenges in novel and harsh environments, including altered precipitation regimes, salinity, extreme temperatures, increased atmospheric CO2, nutrient deficiency, heavy metals, and oxygen. Drought remains a major constraint to crop productivity and meeting food demand, with the frequency, intensity, and duration of drought expected to raise in the coming century. The “cry for help” hypothesis proposes that timely recruiting of the microbiome by plants may confer benefits in stress alleviation, plant growth, fitness, and health. The root-associated microbiome harbors 10–100 times more functional genes than the host, which can significantly stimulate the metabolic and genetic potential of plant–microbiome assembly. However, cross-talk among drought and the root-associated microbes, and among the root-associated microbiome and the host-plant, is less well understood. Understanding the molecular aspect of multiple mechanisms by which microbes associate with plants during drought stress is of fundamental importance in plant biology and agriculture. In this review, we examine the progress in research on the response of plant and its microbiome assemblages and interactions to drought stress, including the impact of drought and root exudates on host resilience. We delve into the potential of ‘omics’ technologies to unravel the signaling networks underlying these interactions and the multiway interactions that occur among the host and its associated microbiome. We then discuss the shortfalls, challenges, and future research directions in this field. Overall, we argue that harnessing/manipulating the crop microbiome presents a promising strategy for improving agricultural systems in the face of global climate change

Improvement of nutritional quality of greenhouse-grown lettuce by arbuscular mycorrhizal fungi is conditioned by the source of phosphorus nutrition

The improvement of the nutritional quality of lettuce by its association with arbuscular mycorrhizal fungi (AMF) has been recently reported in a previous study. The aim of this research was to evaluate if the fertilization with three P sources differing in water solubility affects the effectiveness of AMF for improving lettuce growth and nutritional quality. The application of either water-soluble P sources (Hewitt's solution and single superphosphate) or the water-insoluble (WI) fraction of a “rhizosphere-controlled fertilizer” did not exert negative effects on the establishment of the mycorrhizal symbiosis. AMF improved lettuce growth and nutritional quality. Nevertheless, the effect was dependent on the source of P and cultivar. Batavia Rubia Munguía (green cultivar) benefited more than Maravilla de Verano (red cultivar) in terms of mineral nutrients, total soluble sugars, and ascorbate contents. The association of lettuce with AMF resulted in greater quantities of anthocyanins in plants fertilized with WI, carotenoids when plants received either Hewitt's solution or WI, and phenolics regardless of the P fertilizer applied

Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action

Sánchez-López, Ángela María et al.It is known that volatile emissions from some beneficial rhizosphere microorganisms promote plant growth. Here we show that volatile compounds (VCs) emitted by phylogenetically diverse rhizosphere and non-rhizhosphere bacteria and fungi (including plant pathogens and microbes that do not normally interact mutualistically with plants) promote growth and flowering of various plant species, including crops. In Arabidopsis plants exposed to VCs emitted by the phytopathogen Alternaria alternata, changes included enhancement of photosynthesis and accumulation of high levels of cytokinins (CKs) and sugars. Evidence obtained using transgenic Arabidopsis plants with altered CK status show that CKs play essential roles in this phenomenon, because growth and flowering responses to the VCs were reduced in mutants with CK-deficiency (35S:AtCKX1) or low receptor sensitivity (ahk2/3). Further, we demonstrate that the plant responses to fungal VCs are light-dependent. Transcriptomic analyses of Arabidopsis leaves exposed to A. alternata VCs revealed changes in the expression of light- and CK-responsive genes involved in photosynthesis, growth and flowering. Notably, many genes differentially expressed in plants treated with fungal VCs were also differentially expressed in plants exposed to VCs emitted by the plant growth promoting rhizobacterium Bacillus subtilis GB03, suggesting that plants react to microbial VCs through highly conserved regulatory mechanisms.This work was partially supported by the Comisión Interministerial de Ciencia y Tecnología and Fondo Europeo de Desarrollo Regional (Spain) (grant numbers BIO2010-18239 and BIO2013- 49125-C2-1-P), the Government of Navarra (grant number IIM010491.RI1), the I-Link0939 project from the Ministerio de Economía y Competitividad, the Ministry of Education, Youth and Sports of the Czech Republic (Grant L01204 from the National Program of Sustainability) and Palacky University institutional support. AM S-L and P G-G gratefully acknowledge predoctoral fellowships from the Spanish Ministry of Science and Innovation. M B and G A acknowledge post-doctoral fellowships awarded by the Public University of Navarra.Peer reviewe

Soil application of volatile compounds emitted by Alternaria alternata enhance yield of pepper plants cultured under greenhouse conditions

Póster presentado en el 2nd World Congress on the use of Biostimulants in Agriculture, celebrado en Florencia del 16 al 19 de noviembre de 2015.Peer Reviewe

Characterization of multiple SPS knockout mutants reveals redundant functions of the four Arabidopsis sucrose phosphate synthase isoforms in plant viability, and strongly indicates that enhanced respiration and accelerated starch turnover can alleviate the blockage of sucrose biosynthesis

We characterized multiple knock-out mutants of the four Arabidopsis sucrose phosphate synthase (SPSA1, SPSA2, SPSB and SPSC) isoforms. Despite their reduced SPS activity, spsa1/spsa2, spsa1/spsb, spsa2/spsb, spsa2/spsc, spsb/spsc, spsa1/spsa2/spsb and spsa2/spsb/spsc mutants displayed wild type (WT) vegetative and reproductive morphology, and showed WT photosynthetic capacity and respiration. In contrast, growth of rosettes, flowers and siliques of the spsa1/spsc and spsa1/spsa2/spsc mutants was reduced compared with WT plants. Furthermore, these plants displayed a high dark respiration phenotype. spsa1/spsb/spsc and spsa1/spsa2/spsb/spsc seeds poorly germinated and produced aberrant and sterile plants. Leaves of all viable sps mutants, except spsa1/spsc and spsa1/spsa2/spsc, accumulated WT levels of nonstructural carbohydrates. spsa1/spsc leaves possessed high levels of metabolic intermediates and activities of enzymes of the glycolytic and tricarboxylic acid cycle pathways, and accumulated high levels of metabolic intermediates of the nocturnal starch-to-sucrose conversion process, even under continuous light conditions. Results presented in this work show that SPS is essential for plant viability, reveal redundant functions of the four SPS isoforms in processes that are important for plant growth and nonstructural carbohydrate metabolism, and strongly indicate that accelerated starch turnover and enhanced respiration can alleviate the blockage of sucrose biosynthesis in spsa1/spsc leaves.This work was partially supported by the Comisión Interministerial de Ciencia y Tecnología and Fondo Europeo de Desarrollo Regional (Spain) [grant numbers BIO2010-18239, BIO2013-49125-C2-1-P, BIO2008-02292 and BIO2011-28847-C02-02]. A.M.S-L. acknowledges a predoctoral fellowship from the Spanish Ministry of Science and Innovation. M.B. acknowledges a post-doctoral fellowship from the Public University of Navarra.Peer Reviewe

Volatile compounds emitted by the plant pathogen Alternaria alternata promote photosynthesis, growth and accumulation of high levels of starch in Arabidopsis through pPGI dependent and independent cytokinin biosynthetic processes

Póster presentado en el XXI Reunión de la Sociedad Española de Fisiología Vegetal y el XIV Congreso Hispano-Luso Fisiología Vegetal, celebrado en Toledo del 14 al 17 de junio de 2015.Peer Reviewe

Plant responses to fungal volatiles involve global posttranslational thiol redox proteome changes that affect photosynthesis

Microorganisms produce volatile compounds (VCs) that promote plant growth and photosynthesis through complex mechanisms involving cytokinin (CK) and abscisic acid (ABA). We hypothesized that plants' responses to microbial VCs involve posttranslational modifications of the thiol redox proteome through action of plastidial NADPH-dependent thioredoxin reductase C (NTRC), which regulates chloroplast redox status via its functional relationship with 2-Cys peroxiredoxins. To test this hypothesis, we analysed developmental, metabolic, hormonal, genetic, and redox proteomic responses of wild-type (WT) plants and a NTRC knockout mutant (ntrc) to VCs emitted by the phytopathogen Alternaria alternata. Fungal VC-promoted growth, changes in root architecture, shifts in expression of VC-responsive CK- and ABA-regulated genes, and increases in photosynthetic capacity were substantially weaker in ntrc plants than in WT plants. As in WT plants, fungal VCs strongly promoted growth, chlorophyll accumulation, and photosynthesis in ntrc–Δ2cp plants with reduced 2-Cys peroxiredoxin expression. OxiTRAQ-based quantitative and site-specific redox proteomic analyses revealed that VCs promote global reduction of the thiol redox proteome (especially of photosynthesis-related proteins) of WT leaves but its oxidation in ntrc leaves. Our findings show that NTRC is an important mediator of plant responses to microbial VCs through mechanisms involving global thiol redox proteome changes that affect photosynthesis.Comisión Interministerial de Ciencia y Tecnología BIO2013‐ 49125‐C2‐1‐P, BIO2017‐85195‐C2‐1‐P, BIO2016‐78747‐PEuropean Regional Development CZ.02.1.01/0.0/0.0/16_019/0000827Ministry of Education, Youth and Sport of the Czech Republic LO1204Japan Society for the Promotion of Sciences 15H02486Gobierno de Navarra P1004 PROMEBIO, P1044 AGROEST

Soil application of volatile compounds emitted by the plant pathogen Alternaria alternata enhance yield of pepper plants cultured under greenhouse conditions

Póster presentado en la International Conference "Plant Biotechnology: Green for Good III", celebrada en Olomouc (República Checa) del 15 al 18 de junio de 2015.Peer Reviewe

Volatile compounds emitted by the plant pathogen Alternaria alternata enhance photosynthesis and promote growth of Arabidopsis by increasing cytokinin production

Póster presentado en el Fresh & glycoprotein symposium, celebrado en Japón en septiembre de 2015.Peer Reviewe