Group2. Biochemistry and Molecular Biology of Plant Metabolic and Developmental Pathways

C. EXPERIMENTAL PLAN

1. Metabolic and Regulatory Aspects of Seed Quality and Germination. Elucidation of biochemical and developmental pathways which have a key role in seed development, germination and nutritional quality form the basis of the research conducted in the Dyer and Raboy laboratories, respectively.

  • a. Starch Biosynthesis. The research conducted in the Anderson lab will define the physiological and molecular regulation of starch biosynthesis in seed tissue of barley. This is of particular importance in barley as the starch contained in the endosperm constitutes at least 50 to 60% of the weight of the barley seed and has a significant role in whether barley is used as a feed stock or for malt production by the brewing industry. Starch is synthesized by a complex multi-step pathway which is divided between the cytosol and plastid (Tobias et al. 1992). A number of studies have shown that in leaf tissue starchbiosynthesis is controlled through allosteric regulation of ADPglucose pyrophosphorylase by 3-PGA and Pi levels (Heldt et al. 1977; Preiss 1988; Beck and Ziegler 1989). However, it is not clear if starch biosynthesis in controlled by the same manner in leaf and endosperm (storage) tissue because of key differences in starch metabolism between leaf and non-photosynthetic tissue (Anderson et al. 1990). Several recent reports suggest that there are at least two regulatory mechanisms (at the gene expression and enzyme activity levels) which control starch biosynthesis and hence carbohydrate metabolism in non-photosynthetic tissue (Koch et al. 1992; Muller-Rober etal. 1990; Salanoubat and Belliard 1989).

  • Two approaches to studying starch biosynthesis are being taken. The first is to study the starch biosynthetic pathway at the biochemical and molecular levels. The genes which encode enzymes active in the cytosol and amyloplast and at the beginning, middle, and end of the starch biosynthetic pathway (sucrose synthase, ADPglucose pyrophosphorylase, and granular-bound starch synthase) have been cloned from maize, spinach, wheat, rice, and potato (Nakata et al. 1991; Olive et al. 1989; Preiss 1988; Shure et al. 1983; Werr et al. 1985; Yu et al. 1992). Consequently, using heterologous probes and PCR-based cloning it is now possible to isolate these genes from barley and study the mechanisms of their regulation. The transcript levels of these genes will be correlated to enzyme activity levels during barley kernel development. This should indicate the degree of coordinant regulation of the starch biosynthetic pathway at the gene and enzyme levels at discreet developmental timepoints and throughout seed development. These studies will begin to define the pathway regulating starch synthesis during development. The promoters of these genes will also be analyzed which will lead to the identification of regulatory factors and genes which control starch biosynthesis. The second approach is to isolate mutants, through sodium azide mutagenesis (Nilan et al. 1975), which perturb starch synthesis or genes regulating starch synthesis. Shrunken seed mutations obtained from these populations will be examined biochemically to determine if the lesion is in a specific starch synthesis gene or at some undefined and perhaps regulatory loci. These studies will genetically and molecularly define the starch biosynthetic and regulatory pathways in barley kernels.

  • b. Phytic Acid Synthesis. The main goal of the Raboy lab is to advance the genetics and biochemistry of phytic acid synthesis in higher plants. Phytic acid (myo- inositol hexakisphosphate) is the storage form of phosphorus (P) in seeds, typically representing approximately 75% of seed total P (Raboy 1990). It is deposited during seed development as the mixed "phytate" salts of various mineral cations. The regulation of phytic acid synthesis is probably the mechanism by which both P and mineral concentration and distribution is regulated during seed development.

    Our current objectives include the isolation and characterization of mutations which specifically perturb the accumulation of seed phytic acid, and the identification and purification of enzymes implicated in seed phytic acid synthesis. These are prerequisites to achieving various basic and applied long term goals. Our studies focus on three cereal crops; barley, wheat and maize. The specific objective of this proposal is to isolate and begin the study of barley phytic acid mutants.

    We have isolated two maize mutants, termed low phytic acid 1 (lpa1) and lpa2, in which kernel phytic acid is reduced (by about 66% and 33%, respectively), but which display no other obvious change in kernel phenotype or plant growth habit (unpublished data). These mutants were found using a relatively time-consuming assay for phytic acid. In both cases the observed reduction in kernel phytic acid is essentially entirely accounted for by an increase in inorganic P (Pi). It is interesting that this massiveincrease in Pi has little or no effect on kernel phenotype. We have also identified 1L-myo-inositol 1-monophosphate kinase activity, which we hypothesize catalyzes an early step inphytic acid synthesis, in developing wheat kernels (unpublished data). Optimization of the recovery of this activity in crude extracts and the development of a purification scheme for this activity is currently in progress.

    Based on the maize work, we propose to screen for phytic acid mutants in a population of chemically-induced mutants in barley (recently produced by Co-PI Anderson) by first screening for mutants which substantially increase kernel Pi. This approach should be relatively rapid. We will initially screen to identify M2 families containing kernels which display substantial increases in Pi above that typically observed in wild-type kernels, using a modification of the method of Chen et al (1956). M2 families thus identified will be further analyzed using a High Voltage Paper Electrophoresis (HVPE) methodwhich provides optimal fractionation of Pi, and the various myo-inositol phosphates including phytic acid (Raboy et al. 1990). Any phytic acid mutants thus identified will then be the subject of numerous studies:

    1) to accurately quantify kernel phytic acid, phosphorus
    and mineral fractions; 
    2) to study their inheritance and map location; 
    3) to assay their effect on seed function and physiology
    including mineral distribution; 
    4) to study their biochemistry (do they represent lesions in
    kinase genes, or in other functions such as metabolite
    transport?). 

  • c. Regulation of Seed Dormancy. The molecular regulation of seed dormancy, a unique form of developmental arrest in plants, is being investigated in the Dyer laboratory. The imposition of dormancy during embryogenesis is most likely regulated by endogenous levels of the hormone abscisic acid (ABA), and even though mechanisms controlling maintenance and release from dormancy in mature seeds are not understood, several lines of evidence support the idea that dormancy is imposed during early imbibition. Measurements of respiration (Simmonds and Simpson 1971), protein synthesis (Cuming and Osborne 1978), and water uptake kinetics (Hegarty 1978) indicate that imbibing seeds complete several early steps towards germination before progress is interrupted. Likewise, expression of several ABA-responsive mRNAs persists longer in dormant wheat (Morris et al. 1991), barley (Heck and Ho 1991), and Bromus secalinus (Goldmark et al. 1992) embryos than in nondormant embryos during imbibition, suggesting that dormancy is actively imposed. Thus, during early imbibition, dormancy-associated genes may be differentially expressed and their products selectively repress key metabolic and/or regulatory processes, preventing germination.

    The Dyer laboratory has recently shown using in vitro translation and two-dimensional gel electrophoresis that certain mRNAs and soluble proteins are more highly expressed in dormant Avena fatua embryos than in nondormant embryos during early imbibition (Dyer 1992). Differential expression is visible within 3 hours of imbibition and remains elevated through 12 hours, but dormancy-associated mRNAs return to equivalent levels in dormant and nondormant embryos after 24 hours. To isolate genes thus temporally regulated during early imbibition, cDNA libraries were constructed using mRNA isolated from dormant and nondormant embryos imbibed for 6 hours. After subtraction hybridization, 300 colonies were isolated based on differential hybridization, from which nine clones have been selected for preliminary studies. Comparison of the 375 bp open reading frame of clone S21G5 with DNA databases shows that the A. fatua clone possesses 54% identity in a 211 bp overlap with the open reading frame of a transmembrane transport protein (Van Hove et al. 1990) and 62% identity in a 71 bp overlap with a nuclear pore glycoprotein (Wozniak et al. 1989), suggesting the presence of membrane spanning domains.

    Dormancy-associated cDNA clones will be characterized on three levels. Gene expression will be quantified in northern hybridization experiments to determine:

     
  • a) expression levels in dormant and nondormant embryos,
  • b) timing and length of expression during imbibition,
  • c) tissue specificity, and
  • d) the effect of known dormancy-breaking treatments on expression. cDNAs will be checked for cross-hybridization with several classes of genes known to be expressed during exposure to ABA and/or in response to stresses associated with early germination, including rab, dehydrin, Em, and others. Clones determined to be of interest from the above experiments will be sequenced and compared to DNA and protein sequence databases for preliminary leads on identification. Deduced protein sequences will be analyzed for transcriptional regulatory protein consensus motifs and putative membrane-spanning domains. Selected cDNA clones will be used to isolate their respective genomic clones from A. fatua and Hordeum vulgare libraries for analysis of regulatory domains. Flanking regions will be used as substrates for nuclear protein extracts in gel shift assays to assay for the presence of potential cis-acting domains. Functional studies of selected dormancy-specific clones will be conducted in transgenic plants. Antisense constructions controlled by their respective promoters will be introduced into embryogenic A. fatua and H. vulgare callus cultures through particle bombardment. Blocking gene expression should lead to loss of dormancy during imbibition of transgenic mature embryos.
  • 2. Plant Receptors and Signal Transduction. Two members of the group are investigating plant receptors and their mechanisms of action. Characterization of the phytochrome photoreceptor family is the major objective of research in the Sharrock laboratory. The Stout lab is studying membrane transport systemsas they relate to the receptor for the phytotoxin fusicoccin (FC) and rapid phytochrome-mediated responses.

  • a. Phytochrome structure and function. The Sharrock laboratory is specificallyinterested in the question of how the light cues that control plant physiological and developmental processes are perceived. This is addressed through the isolation, characterization, and manipulation of plant photoreceptor genes. The first plant regulatory photoreceptor to be isolated, and to date the best characterized, is the red/far red light- responsive chromoprotein phytochrome (Quail 1991; Smith and Whitelam 1990). Working with the small model plant Arabidopsis thaliana, it has been shown that "phytochrome" is in fact a family of five related but structurally diverse apoproteins, coded for by five phy genes, and their associated chromophores (Sharrock and Quail 1989; unpublished). The presence of an extensive phytochrome receptor family in plants suggests that the control of diverse red light-induced physiological, metabolic, and developmental responses may reflect differential roles of specific photoreceptor types.

  • Future work on this project will emphasize analysis of the regulation and individual functions of the five Arabidopsis phytochromes. Using the polymerase chain reaction (PCR), phytochrome gene families homologous to the Arabidopsis family have been detected in a wide variety of flowering plants including the agriculturally-important monocot grain species. This is significant in that it suggests that much of what is learned from analysis of the phy genes in Arabidopsis should be applicable to higher plants in general. In Arabidopsis, all five phy genes are expressed at the level of mRNA and, using monoclonal antibodies, three of the five have been shown to be expressed at the protein level (Somers et al. 1991). One future goal in this laboratory is to generate additional monoclonal antibodies that are specific to each of the five phy gene protein products. Using transcript-specific nucleic acid hybridization probes and these antibodies, it will be possible to characterize in detail the tissue distribution and developmental regulation of the phy mRNAs and proteins.

    In an effort to define functions for the phytochromes, levels of these receptors in various photomorphogenic mutants of Arabidopsis have been analyzed. A mutant showing aberrant red light regulation of seedling stem elongation was found to be specifically deficient for one of the low abundance light-stable phytochromes, phyB (Somers et al. 1991). Current work on this project involves molecular analysis of the mutant and transgenic complementation of the mutant phenotype with a recombinant phyB gene introduced into mutant plants via Agrobacterium-mediated transformation. Assignment of a physiological function in the control of seedling growth to phyB phytochrome is a major step forward in understanding this receptor family. Further analysis of the Arabidopsis phytochrome family will include attempts to specifically block expression of individual phy genes in transgenic plants using antisense RNA and investigation of the patterns of expression of the various phy genes using phy promoter regions fused to a reporter gene.

  • b. Membrane transport and signal transduction. The Stout laboratory studies plant membrane transport, particularly its relationship to cellular mechanisms regulating plant development. This has included work on proton-translocating ATPases, putative hormone and phytotoxin receptor proteins, receptor-mediated endocytosis, and tissue-specific plasma membrane proteins. The proton-pumping ATPases in the plasma membrane and the tonoplast are primary transport systems in plant cells and their regulation is critical to plant cell physiology (Serrano 1989). The phytotoxin fusicoccin (FC) rapidly stimulates the plasma membrane H+-ATPase and cell enlargement through an FC receptor that is localized in the membrane but is distinct from the ATPase (Stout and Cleland 1980; Stout 1988). Future work on this system will focus on characterization of the FC receptor and its connection to the H+-ATPase using FC-insensitive mutants of Arabidopsis.

  • In a collaboration between the Stout and Sharrock laboratories, the role of calcium-mediated signal transduction in rapid phytochrome responses, in particular red-light induced leaf movement, will be investigated. Such a rapid physiological effect of phytochrome does not involve transcriptional regulation, thus phytochrome is modulating an intracellular system already in place. Phytochrome may act by elevating the cytosolic free Ca++ concentration (Ca++cyt). Secondary effects may include opening of calcium-gated potassium channels in the membrane (affecting turgor), reorientation of cytoskeletal elements (via the Ca++-modulated protein annexin), and the activation of elements of the inositol-phospholipid second messenger system (Leonard and Hepler 1990; Roberts and Harmon 1992). Using currently available techniques (such as injection of Ca++-sensitive fluorescent dyes) to determine Ca++cyt, the earliest effects of red light stimulation of Ca++cyt in the leaf motor cells will be examined in a variety of leguminous plants.