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1.
Mol Plant ; 17(7): 1073-1089, 2024 Jul 01.
Article in English | MEDLINE | ID: mdl-38807367

ABSTRACT

The gray mold fungus Botrytis cinerea is a necrotrophic pathogen that causes diseases in hundreds of plant species, including high-value crops. Its polyxenous nature and pathogenic success are due to its ability to perceive host signals in its favor. In this study, we found that laticifer cells of Euphorbia lathyris are a source of susceptibility factors required by B. cinerea to cause disease. Consequently, poor-in-latex (pil) mutants, which lack laticifer cells, show full resistance to this pathogen, whereas lot-of-latex mutants, which produce more laticifer cells, are hypersusceptible. These S factors are triterpenoid saponins, which are widely distributed natural products of vast structural diversity. The downregulation of laticifer-specific oxydosqualene cyclase genes, which encode the first committed step enzymes for triterpene and, therefore, saponin biosynthesis, conferred disease resistance to B. cinerea. Likewise, the Medicago truncatula lha-1 mutant, compromised in triterpenoid saponin biosynthesis, showed enhanced resistance. Interestingly, the application of different purified triterpenoid saponins pharmacologically complemented the disease-resistant phenotype of pil and hla-1 mutants and enhanced disease susceptibility in different plant species. We found that triterpenoid saponins function as plant cues that signal transcriptional reprogramming in B. cinerea, leading to a change in its growth habit and infection strategy, culminating in the abundant formation of infection cushions, the multicellular appressoria apparatus dedicated to plant penetration and biomass destruction in B. cinerea. Taken together, these results provide an explanation for how plant triterpenoid saponins function as disease susceptibility factors to promote B. cinerea pathogenicity.


Subject(s)
Botrytis , Plant Diseases , Saponins , Triterpenes , Botrytis/pathogenicity , Saponins/pharmacology , Saponins/metabolism , Plant Diseases/microbiology , Triterpenes/metabolism , Triterpenes/pharmacology , Euphorbia/microbiology , Euphorbia/metabolism , Disease Resistance/genetics , Medicago truncatula/microbiology , Medicago truncatula/metabolism , Medicago truncatula/genetics , Mutation , Gene Expression Regulation, Plant
2.
New Phytol ; 219(4): 1467-1479, 2018 09.
Article in English | MEDLINE | ID: mdl-29878406

ABSTRACT

Laticifers are specialized plant cells capable of indefinite elongation that ramify extensively and are responsible for latex biosynthesis and accumulation. However, the mechanisms underlying laticifer cell differentiation, growth and production of latex remain largely unknown. In a search for mutants showing enhanced accumulation of latex we identified two LOT OF LATEX (LOL) loci in Euphorbia lathyris. lol2 and lol5 mutants show enhanced production of latex contained within laticifer cells. The recessive lol2 mutant carries increased biosynthesis of the plant hormone jasmonoyl-isoleucine (JA-Ile) and therefore establishes a genetic link between jasmonic acid (JA) signaling and latex production in laticifers. Instead, heightened production of latex in lol5 plants obeys to enhanced proliferation of laticifer cells. Phylogenetic analysis of laticifer-expressed genes in E. lathyris and in two other latex-bearing species, Euphorbia corallioides and Euphorbia palustris, allowed the identification of canonical JA responsive elements present in the gene promoter regions of laticifer marker genes. Moreover, we identified that the hormone JA functions not as a morphogen for laticifer differentiation but as a trigger for the fill out of laticifers with latex and the associated triterpenoids. The identification of LOL loci represents a further step towards the understanding of mechanisms controlling latex production in laticifer cells.


Subject(s)
Euphorbia/genetics , Genes, Plant , Genetic Loci , Latex/metabolism , Plant Proteins/genetics , Cyclopentanes/pharmacology , Gene Expression Regulation, Plant/drug effects , Mutation/genetics , Oxylipins/pharmacology , Phylogeny , Plant Proteins/metabolism , Promoter Regions, Genetic/genetics , Seedlings/drug effects , Seedlings/genetics , Triterpenes/metabolism
3.
Plant Signal Behav ; 12(7): e1300743, 2017 07 03.
Article in English | MEDLINE | ID: mdl-28718699

ABSTRACT

In the latex-bearing plants, the laticiferous system is the tubing structure that contains the latex and is constituted of living cells (laticifers). While laticifers are present only in a small percentage of the flowering plant species, they represent a type of specialized tissue within the plant where a myriad of metabolites are synthesized, some of them of considerable commercial importance. In this mini-review we synopsize the present knowledge about laticifer cells and discuss about their particular features as well as some evolutionary and ecophysiological cues and the potential exploitation of the knowledge generated around this peculiar type of plant cell. We illustrate some of these questions with the experience in Euphorbia lathyris laticifers and latex.


Subject(s)
Euphorbia/cytology , Latex , Euphorbia/physiology
4.
Plant Physiol ; 172(2): 1032-1044, 2016 10.
Article in English | MEDLINE | ID: mdl-27468995

ABSTRACT

Laticifer cells are specialized plant cells that synthesize and accumulate latex. Studies on laticifers have lagged behind in recent years, and data regarding the functional role of laticifers and their fitness benefit still remain elusive. Laticifer differentiation and its impact on plant growth and development also remain to be investigated. Here, cellular, molecular, and genetic tools were developed to examine the distribution, differentiation, ontogeny, and other characteristic features, as well as the potential developmental role of laticifer cells in the latex-bearing plant Euphorbia lathyris. The organization of the laticiferous system within the E. lathyris plant body is reported, emerging as a single elongated and branched coenocytic cell, constituting the largest cell type existing in plants. We also report the ontogeny and organization of laticifer cells in the embryo and the identification of a laticifer-associated gene expression pattern. Moreover, the identification of laticifer- and latex-deficient mutants (pil mutants) allowed for the identification of distinct loci regulating laticifer differentiation, growth, and metabolic activity. Additionally, pil mutants revealed that laticifer cells appear nonessential for plant growth and development, thus pointing toward their importance, instead, for specific ecophysiological adaptations of latex-bearing plants in natural environments.


Subject(s)
Euphorbia/genetics , Gene Expression Regulation, Plant , Latex/biosynthesis , Plant Proteins/genetics , Cell Lineage/genetics , Cotyledon/cytology , Cotyledon/genetics , Cotyledon/metabolism , Euphorbia/cytology , Euphorbia/metabolism , Gene Expression Profiling/methods , Latex/analysis , Microscopy, Electron, Scanning , Mutation , Plant Leaves/cytology , Plant Leaves/genetics , Plant Leaves/metabolism , Plant Proteins/metabolism , Plant Stems/cytology , Plant Stems/genetics , Plant Stems/metabolism , Reverse Transcriptase Polymerase Chain Reaction , Seedlings/cytology , Seedlings/genetics , Seedlings/metabolism , Seeds/cytology , Seeds/genetics , Seeds/metabolism , Terpenes/analysis , Terpenes/metabolism
5.
Plant Physiol ; 155(4): 1920-35, 2011 Apr.
Article in English | MEDLINE | ID: mdl-21282403

ABSTRACT

In this study, we show that the Arabidopsis (Arabidopsis thaliana) transcription factor MYB46, previously described to regulate secondary cell wall biosynthesis in the vascular tissue of the stem, is pivotal for mediating disease susceptibility to the fungal pathogen Botrytis cinerea. We identified MYB46 by its ability to bind to a new cis-element located in the 5' promoter region of the pathogen-induced Ep5C gene, which encodes a type III cell wall-bound peroxidase. We present genetic and molecular evidence indicating that MYB46 modulates the magnitude of Ep5C gene induction following pathogenic insults. Moreover, we demonstrate that different myb46 knockdown mutant plants exhibit increased disease resistance to B. cinerea, a phenotype that is accompanied by selective transcriptional reprogramming of a set of genes encoding cell wall proteins and enzymes, of which extracellular type III peroxidases are conspicuous. In essence, our results substantiate that defense-related signaling pathways and cell wall integrity are interconnected and that MYB46 likely functions as a disease susceptibility modulator to B. cinerea through the integration of cell wall remodeling and downstream activation of secondary lines of defense.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/genetics , Botrytis/pathogenicity , Plant Diseases/genetics , Transcription Factors/metabolism , Arabidopsis/immunology , Arabidopsis/microbiology , Arabidopsis Proteins/genetics , Binding Sites , Cell Wall/chemistry , Gene Expression Profiling , Gene Expression Regulation, Plant , Host-Pathogen Interactions , Immunity, Innate , Lignin/metabolism , Mutagenesis, Insertional , Oligonucleotide Array Sequence Analysis , Plant Diseases/immunology , Plant Diseases/microbiology , Plant Immunity , Plants, Genetically Modified/genetics , Plants, Genetically Modified/immunology , Plants, Genetically Modified/microbiology , Promoter Regions, Genetic , RNA, Plant , Transcription Factors/genetics
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