Jasmonates: An Update on Biosynthesis, Signal Transduction and Action in Plant Stress Response, Growth and Development

INTRODUCTION. Internal Organization of the Plant Body. Summary of Types of Cells and Tissues. General References. DEVELOPMENT OF THE SEED PLANT. The Embryo. From embryo to the Adult Plant. Apical Meristems and Their Derivatives. Differentiation, Specialization, and Morphogenesis. References. THE CELL. Cytoplasm. Nucleus. Plastids. Mitochondria. Microbodies. Vacuoles. Paramural Bodies. Ribosomes. Dictyosomes. Endoplasmic Reticulum. Lipid Globules. Microtubules. Ergastic Substances. References. CELL WALL. Macromolecular Components and Their Organization in the Wall. Cell Wall Layers. Intercellular Spaces. Pits, Primary Pit--Fields, and Plasmodesmata. Origin of Cell Wall During Cell Division. Growth of Cell Wall. References. PARENCHYMA AND COLLENCHYMA. Parenchyma. Collenchyma. References. SCLERENCHYMA. Sclereids. Fibers. Development of Sclereids and Fibers. References. EPIDERMIS. Composition. Developmental Aspects. Cell Wall. Stomata. Trichomes. References. XYLEM: GENERAL STRUCTURE AND CELL TYPES. Gross Structure of Secondary Xylem. Cell Types in the Secondary Xylem. Primary Xylem. Differentiation of Tracheary Elements. References. XYLEM: VARIATION IN WOOD STRUCTURE. Conifer Wood. Dicotyledon Wood. Some Factors in Development of Secondary Xylem. Identification of Wood. References. VASCULAR CAMBIUM. Organization of Cambium. Developmental Changes in the Initial Layer. Patterns and Causal Relations in Cambial Activity. References. PHLOEM. Cell Types. Primary Phloem. Secondary Phloem. References. PERIDERM. Structure of Periderm and Related Tissues. Development of Periderm. Outer Aspect of Bark in Relation to Structure. Lenticels. References. SECRETORY STRUCTURES. External Secretory Structures. Internal Secretory Structures. References. THE ROOT: PRIMARY STATE OF GROWTH. Types of Roots. Primary Structure. Development. References. THE ROOT: SECONDARY STATE OF GROWTH AND ADVENTITIOUS ROOTS. Common Types of Secondary Growth. Variations in Secondary Growths. Physiologic Aspects of Secondary Growth in Roots. Adventitious Roots. References. THE STEM: PRIMARY STATE OF GROWTH. External Morphology. Primary Structure. Development. References. THE STEM: SECONDARY GROWTH AND STRUCTURAL TYPES. Secondary Growth. Types of Stems. References. THE LEAF: BASIC STRUCTURE AND DEVELOPMENT. Morphology. Histology of Angiosperm Leaf. Development. Abscission. References. THE LEAF: VARIATIONS IN STRUCTURE. Leaf Structure and Environment. Dicotyledon Leaves. Monocotyledon Leaves. Gymnosperm Leaves. References. THE FLOWER: STRUCTURE AND DEVELOPMENT. Concept. Structure. Development. References. THE FLOWER: REPRODUCTIVE CYCLE. Microsporogenesis. Pollen. Male Gametophyte. Megasporogenesis. Female Gametophyte. Fertilization. References. THE FRUIT. Concept and Classification. The Fruit Wall. Fruit Types. Fruit Growths. Fruit Abscission. References. THE SEED. Concept and Morphology. Seed Development. Seed Coat. Nutrient Storage Tissues. References. EMBRYO AND SEEDLING. Mature Embryo. Development of Embryo. Classification of Embryos. Seedling. References. Glossary. Index.

Anatomy of Seed Plants

Plant responses to many biotic and abiotic stresses are orchestrated locally and systemically by signaling molecules known as the jasmonates (JAs). JAs also regulate such diverse processes as pollen maturation and wound responses in Arabidopsis. Here we review recent advances in our understanding of

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The Jasmonate Signal Pathway

Despite its importance in a variety of plant defense responses, our understanding of how jasmonic acid (JA) functions at the biochemical level is limited. Several amino acid conjugates of JA were tested for their ability to complement the JA-insensitive Arabidopsis thaliana mutant jar1-1. Unlike free JA, JA-Ile inhibited root growth in jar1-1 to the same extent as in the wild type, whereas JA-Val, JA-Leu, and JA-Phe were ineffective inhibitors in both genotypes. Thin-layer chromatography and gas chromatography–mass spectrometry (GC-MS) analysis of products produced in vitro by recombinant JAR1 demonstrated that this enzyme forms JA-amido conjugates with several amino acids, including JA-Ile. JA-Val, -Leu, -Ile, and -Phe were each quantified in Arabidopsis seedlings by GC-MS. JA-Ile was found at 29.6 pmole g−1 fresh weight (FW) in the wild type but was more than sevenfold lower in two jar1 alleles. JA-Leu, -Val, and -Phe were present at only low levels in both genotypes. Expression of wild-type JAR1 in transgenic jar1-1 plants restored sensitivity to JA and elevated JA-Ile to the same level as in the wild type. The ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) conjugated to JA was also found in plant tissue at 18.4 pmole g−1 FW. JA-ACC was determined not be an effective jasmonate root inhibitor, and surprisingly, was twofold higher in the mutants than in the wild type. This suggests that another JA-conjugating enzyme(s) is present in Arabidopsis. Synthesis of JA-ACC might provide a mechanism to coregulate the availability of JA and ACC for conversion to the active hormones JA-Ile and ethylene, respectively. We conclude that JAR1 is a JA-amino synthetase that is required to activate JA for optimal signaling in Arabidopsis. Plant hormone activation by conjugation to amino acids and the enzymes involved in their formation were previously unknown.

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The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis.

https://arca.igc.gulbenkian.pt/bitstream/10400.7/67/4/Slotkin%20et%20al%202009%20post-print.pdf

Epigenetic Reprogramming and Small RNA Silencing of Transposable Elements in Pollen

We identified Arabidopsis thaliana sterility mutants by screening T-DNA and EMS-mutagenized lines and characterized several male-sterile mutants with defects specific for different anther processes. Approximately 44 and 855 sterile mutants were uncovered from the T-DNA and EMS screens, respectively. Several mutants were studied in detail with defects that included the establishment of anther morphology, microspore production, pollen differentiation, and anther dehiscence. Both non-dehiscencing and late-dehiscencing mutants were identified. In addition, pollenless mutants were observed with either apparent meiotic defects and/or abnormalities in cell layers surrounding the locules. Two mutant alleles were identified for the POLLENLESS3 locus which have defects in functional microspore production that lead to the degeneration of cells within the anther locules. pollenless3–1 contains a T-DNA insertion that co-segregates with the mutant phenotype and pollenless3–2 has a large deletion in the POLLENLESS3 gene. The POLLENLESS3 gene has no known counterparts in the GenBank, but encodes a protein containing putative nuclear localization and protein-protein interaction motifs. The POLLENLESS3 gene was shown recently to be the same as MS5, a previously described Arabidopsis
thaliana male-sterility mutant. Three genes were identified in the POLLENLESS3 genomic region: GENEY, POLLENLESS3, and β9-TUBULIN. The segment of the Arabidopsis
thaliana genome containing the POLLENLESS3 and β9-TUBULIN genes is duplicated and present on a different chromosome. Analysis of the POLLENLESS3 expression pattern determined that the 1.3-kb POLLENLESS3 mRNA is localized specifically within meiotic cells in the anther locules and that POLLENLESS3 mRNA is present only during late meiosis.

Anther developmental defects in Arabidopsis thaliana male-sterile mutants

Male reproductive processes in flowering plants take place in the stamen (Esau, 1977). This sporophytic organ system contains diploid cells that undergo meiosis and produce haploid male spores, or microspores. Microspores divide mitotically and differentiate into multicellular male gametophytes, or pollen grains, that contain the sperm cells. Figures 1 and 2 show that the stamen consists of two morphologically distinct partsthe anther and the filament. The filament is a tube of vascular tissue that anchors the stamen to the flower and serves as a conduit for water and nutrients. By contrast, the anther contains the reproductive and nonreproductive tissues that are responsible for producing and releasing pollen grains so that pollination and fertilization processes can occur within the flower. Figure 1 shows that anther development can be divided into two general phases. During phase 1, the morphology of the anther is established, cell and tissue differentiation occur, and microspore mother cells undergo meiosis. At the end of phase 1, the anther contains most of its specialized cells and tissues, and tetrads of microspores are present within the pollen sacs (Figure 1). During phase 2, pollen grains differentiate, the anther enlarges and is pushed upward in the flower by filament extension, and tissue degeneration, dehiscence, and pollen grain release occur (Figure 1). The cellular processes that regulate anther cell differentiation, establish anther tissue patterns, and cause the anther to switch from a histospecification program (phase l) to a cell degeneration and dehiscence program (phase 2) are not known. The developmental events leading to anther formation and pollen release are exquisitely timed and choreographed (Koltunow et al., 1990; Scott et al., 1991). Cell differentiation and dehiscence events occur in a precise chronological order that correlates with floral bud size (Koltunow et al., 1990; Scott et al., 1991). This permits the mechanisms responsible for cell-type differentiation, tissue degeneration, and cellspecific gene activation within the anther to be explored with relative Base. During the past few years, there has been an explosive burst of interest in anther biology, both as a system to dissect plant developmental processes at the molecular and genetic levels (Koltunow et al., 1990; Gasser, 1991; McCormick,

Anther development: basic principles and practical applications.

delayed dehiscence1 is an Arabidopsis T-DNA mutant in which anthers release pollen grains too late for pollination to occur. The delayed dehiscence1 defect is caused by a delay in the stomium degeneration program. The gene disrupted in delayed dehiscence1 encodes 12-oxophytodienoate reductase, an enzyme in the jasmonic acid biosynthesis pathway. We rescued the mutant phenotype by exogenous application of jasmonic acid and obtained seed set from previously male-sterile plants. In situ hybridization studies showed that during the early stages of floral development, DELAYED DEHISCENCE1 mRNA accumulated within all floral organs. Later, DELAYED DEHISCENCE1 mRNA accumulated specifically within the pistil, petals, and stamen filaments. DELAYED DEHISCENCE1 mRNA was not detected in the stomium and septum cells of the anther that are involved in pollen release. The T-DNA insertion in delayed dehiscence1 eliminated both DELAYED DEHISCENCE1 mRNA accumulation and 12-oxophytodienoate reductase activity. These experiments suggest that jasmonic acid signaling plays a role in controlling the time of anther dehiscence within the flower.

The arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway.

Dehiscence is the terminal step in anther development that releases pollen grains from the wall of each theca at a specific site between the two locules. In tobacco, two groups of cells—the circular cell cluster and the stomium—are required for anther dehiscence and define the position at which pollen is released. The processes responsible for the differentiation of the circular cell cluster and the stomium from cells in specific anther regions are unknown. Nor is it understood what initiates the programmed degeneration of these cell types that ultimately is responsible for pollen release from the anther. We characterized stomium and circular cell cluster differentiation and degeneration using both light and transmission electron microscopy throughout anther development, from the emergence of stamen primordia to anther dehiscence at flower opening. We observed that histological changes within primordium L1 and L2 cells destined to become the stomium and circular cell cluster occur at the same time after the differentiation of surrounding locule regions. Sub-epidermal cells that differentiate into the circular cell cluster divide, enlarge, and generate vacuoles with calcium oxalate crystals prior to any detectable changes in pre-stomium epidermal cells. Differentiation and division of cells that generate the stomium occur after cell degeneration initiates in the circular cell cluster. Prior to dehiscence, the stomium consists of a small set of cytoplasmically dense cells that are easily distinguished from their larger, highly vacuolate epidermal neighbors. Plasmodesmata connections within and between cells of the stomium and circular cell cluster were observed at different developmental stages, suggesting that these cells communicate with each other. Circular cell cluster and stomium cell death is programmed developmentally and occurs at different times. Degeneration of the circular cell cluster occurs first, contributes to the formation of a bilocular anther, and generates the site of anther wall breakage. The stomium cell death process is complete at flower opening and provides an opening for pollen release from each theca. We used laser capture microdissection and real-time quantitative reverse-transcription polymerase chain reactions to demonstrate that stomium cells can be isolated from developing anthers and studied for the presence of specific mRNAs. Our data suggest that a cascade of unique gene expression events throughout anther development is required for the dehiscence program, and that the differentiation of the stomium and circular cell cluster in the interlocular region of the anther probably involves cell signaling processes.

Differentiation and degeneration of cells that play a major role in tobacco anther dehiscence

The processes controlling the differentiation of plant cells are not well understood. Two alternative, but not mutually exclusive, mechanisms probably play a major role in plant-cell differentiation. One mechanism utilizes a position-independent, cell-autonomous differentiation process. The other, employs a position-dependent, cell-cell interaction process that requires signals from neighbouring cells. Cell ablation studies can be used to distinguish between these two models of plant-cell differentiation. In this article we outline a new cell-ablation strategy that utilizes promoters with distinct, but overlapping, cell specificities that are fused with cytotoxic and anticytotoxic structural genes. We present preliminary observations on how this strategy can be used to dissect the events controlling anther development.

Paul M. Sanders

Papers

Anther developmental defects in Arabidopsis thaliana male-sterile mutants

Anther development: basic principles and practical applications.

The arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway.

Differentiation and degeneration of cells that play a major role in tobacco anther dehiscence

A Novel Cell-Ablation Strategy for Studying Plant Development