The role of plastids in plant speciation

Understanding the molecular basis of how new species arise is a central question and prime challenge in evolutionary biology and includes understanding how genomes diversify. Eukaryotic cells possess an integrated compartmentalized genetic system of endosymbiotic ancestry. The cellular subgenomes in nucleus, mitochondria and plastids communicate in a complex way and co-evolve. The application of hybrid and cybrid technologies, most notably those involving interspecific exchanges of plastid and nuclear genomes, has uncovered a multitude of species-specific nucleo-organelle interactions. Such interactions can result in plastome-genome incompatibilities, which can phenotypically often be recognized as hybrid bleaching, hybrid variegation or disturbance of the sexual phase. The plastid genome, because of its relatively low number of genes, can serve as a valuable tool to investigate the origin of these incompatibilities. In this article, we review progress on understanding how plastome-genome co-evolution contributes to speciation. We genetically classify incompatible phenotypes into four categories. We also summarize genetic, physiological and environmental influence and other possible selection forces acting on plastid-nuclear co-evolution and compare taxa providing molecular access to the underlying loci. It appears that plastome-genome incompatibility can establish hybridization barriers, comparable to the Dobzhansky-Muller model of speciation processes. Evidence suggests that the plastid-mediated hybridization barriers associated with hybrid bleaching primarily arise through modification of components in regulatory networks, rather than of complex, multisubunit structures themselves that are frequent targets.     

The role of transporters in supplying energy to plant plastids

The energy status of plant cells strongly depends on the energy metabolism in chloroplasts and mitochondria, which are capable of generating ATP either by photosynthetic or oxidative phosphorylation, respectively. Another energy-rich metabolite inside plastids is the glycolytic intermediate phosphoenolpyruvate (PEP). However, chloroplasts and most non-green plastids lack the ability to generate PEP via a complete glycolytic pathway. Hence, PEP import mediated by the plastidic PEP/phosphate translocator or PEP provided by the plastidic enolase are vital for plant growth and development. In contrast to chloroplasts, metabolism in non-green plastids (amyloplasts) of starch-storing tissues strongly depends on both the import of ATP mediated by the plastidic nucleotide transporter NTT and of carbon (glucose 6-phosphate, Glc6P) mediated by the plastidic Glc6P/phosphate translocator (GPT). Both transporters have been shown to co-limit starch biosynthesis in potato plants. In addition, non-photosynthetic plastids as well as chloroplasts during the night rely on the import of energy in the form of ATP via the NTT. During energy starvation such as prolonged darkness, chloroplasts strongly depend on the supply of ATP which can be provided by lipid respiration, a process involving chloroplasts, peroxisomes, and mitochondria and the transport of intermediates, i.e. fatty acids, ATP, citrate, and oxaloacetate across their membranes. The role of transporters involved in the provision of energy-rich metabolites and in pathways supplying plastids with metabolic energy is summarized here.     

Versatile roles of plastids in plant growth and development

Plastids, found in plants and some parasites, are of endosymbiotic origin. The best-characterized plastid is the plant cell chloroplast. Plastids provide essential metabolic and signaling functions, such as the photosynthetic process in chloroplasts. However, the role of plastids is not limited to production of metabolites. Plastids affect numerous aspects of plant growth and development through biogenesis, varying functional states and metabolic activities. Examples include, but are not limited to, embryogenesis, leaf development, gravitropism, temperature response and plant-microbe interactions. In this review, we summarize the versatile roles of plastids in plant growth and development.     

The ABC of auxin transport: the role of p-glycoproteins in plant development

A surprising outcome of the Arabidopsis genome project was the annotation of a large number of sequences encoding members of the ABC transporter superfamily, including 22 genes encoding the p-glycoprotein (PGP) subfamily. As mammalian PGP orthologs are associated with multiple drug resistance, plant PGPs were initially presumed to function in detoxification, but were soon seen to have a developmental role. Here, we summarise recent studies of plant PGPs indicating that PGPs mediate the cellular and long-distance transport of the plant hormone auxin. One class of PGPs, represented by AtPGP1, catalyze auxin export, while another class with at least one member, AtPGP4, appears to function in auxin import. Current models on the physiological role of PGPs, their functional interaction and their involvement in cell-to cell (polar) auxin transport are discussed.     

Metabolism and transport in non-photosynthetic plastids

Plastids in non-photosynthetic tissue are the site of fattyacid, starch and amino acid synthesis. The intermediates tosupport these activities are imported from the cytoplasm orgenerated by carbohydrate oxidation within the organelle. Thisreview considers the current understanding of the nature ofthe substrates which are transported into such plastids, theinteraction between pathways within the organelle which havea supply and demand relationship, and pathways which potentiallycompete for substrates. Key words: Non-photosynthetic plastids, metabolite transport, starch, fatty acids, nitrogen assimilation     

Auxin in action: signalling, transport and the control of plant growth and development

Hormones have been at the centre of plant physiology research for more than a century. Research into plant hormones (phytohormones) has at times been considered as a rather vague subject, but the systematic application of genetic and molecular techniques has led to key insights that have revitalized the field. In this review, we will focus on the plant hormone auxin and its action. We will highlight recent mutagenesis and molecular studies, which have delineated the pathways of auxin transport, perception and signal transduction, and which together define the roles of auxin in controlling growth and patterning.     

The role of sterols in plant growth and development

Sterols found in all eukaryotic organisms are membrane components which regulate the fluidity and the permeability of phospholipid bilayers. Certain sterols in minute amounts, such as campesterol in Arabidopsis thaliana, are precursors of oxidized steroids acting as growth hormones collectively named brassinosteroids. The crucial importance of brassinosteroids upon growth and development has been established through the study of a set of dwarf mutants affected in brassinosteroid synthesis or perception. Some of these dwarfs are, in fact, deficient in the final steps of sterol biosynthesis and their developmental phenotypes are primarily caused by a depletion in the sterol precursor for brassinosteroids. Recently, the characterization of genes encoding sterol biosynthetic enzymes and the isolation of novel plant lines affected in the expression of those genes, either by insertional or classical mutagenesis, overexpression or cosuppression, have shed new light on the involvement of sterols in biological processes such as embryonic development, cell and plant growth, and fertility, which will be presented and discussed in this review article.     

Proline metabolism and transport in plant development

Proline fulfils diverse functions in plants. As amino acid it is a structural component of proteins, but it also plays a role as compatible solute under environmental stress conditions. Proline metabolism involves several subcellular compartments and contributes to the redox balance of the cell. Proline synthesis has been associated with tissues undergoing rapid cell divisions, such as shoot apical meristems, and appears to be involved in floral transition and embryo development. High levels of proline can be found in pollen and seeds, where it serves as compatible solute, protecting cellular structures during dehydration. The proline concentrations of cells, tissues and plant organs are regulated by the interplay of biosynthesis, degradation and intra- as well as intercellular transport processes. Among the proline transport proteins characterized so far, both general amino acid permeases and selective compatible solute transporters were identified, reflecting the versatile role of proline under stress and non-stress situations. The review summarizes our current knowledge on proline metabolism and transport in view of plant development, discussing regulatory aspects such as the influence of metabolites and hormones. Additional information from animals, fungi and bacteria is included, showing similarities and differences to proline metabolism and transport in plants.     

The role of ethylene in the development of plant form

Ethylene is a gaseous growth factor involved in a diverse arrayof cellular, developmental and stress-related processes in plants.A number of examples of the role played by ethylene in the developmentof form in plants are described; reaction wood formation, floralinduction, sex determination, flooding-induced shoot elongation,and leaf abscission. Recent advances in the understanding ofthe molecular mechanism under-pinning post-pollination perianthwilting in orchids is reviewed. This study indicates that theprocess of post-pollination perianth wilting involves an earlyincrease in sensitivity to endogenous levels of ethylene whichset in motion a chain of events in which ethylene autocatalyticallyinduces its own synthesis in the pistil. Ethylene also inducesthe expression of ACO in the perianth which converts pistil-derivedACC into ethylene which drives the wilting process. Conceptsdrawn from this system are then applied to the Arabidopsis rootepidermis in which ethylene is a positive regulator of roothair development in an effort to come to a mechanistic understandingof the process of pattern formation in this system. Understandingthe molecular basis of the role of ethylene in these model systemswill provide useful paradigms for examining the part playedby ethylene in the diverse array of processes in which thisgrowth factor is involved. Key words: Ethylene, development, plant form     

The role of microbial signals in plant growth and development

Plant growth and development involves a tight coordination of the spatial and temporal organization of cell division, cell expansion and cell differentiation. Orchestration of these events requires the exchange of signaling molecules between the root and shoot, which can be affected by both biotic and abiotic factors. The interactions that occur between plants and their associated microorganisms have long been of interest, as knowledge of these processes could lead to the development of novel agricultural applications. Plants produce a wide range of organic compounds including sugars, organic acids and vitamins, which can be used as nutrients or signals by microbial populations. On the other hand, microorganisms release phytohormones, small molecules or volatile compounds, which may act directly or indirectly to activate plant immunity or regulate plant growth and morphogenesis. In this review, we focus on recent developments in the identification of signals from free-living bacteria and fungi that interact with plants in a beneficial way. Evidence has accumulated indicating that classic plant signals such as auxins and cytokinins can be produced by microorganisms to efficiently colonize the root and modulate root system architecture. Other classes of signals, including N-acyl-L-homoserine lactones, which are used by bacteria for cell-to-cell communication, can be perceived by plants to modulate gene expression, metabolism and growth. Finally, we discuss the role played by volatile organic compounds released by certain plant growth-promoting rhizobacteria in plant immunity and developmental processes. The picture that emerges is one in which plants and microbes communicate themselves through transkingdom signaling systems involving classic and novel signals.Key words: Arabidopsis, alkamides, auxins, quorum-sensing, cytokinins     

The COP9 signalosome and its role in plant development

The COP9 signalosome (CSN) is an evolutionarily conserved multiprotein complex with a role in the regulation of cullin-RING type E3 ubiquitin ligases (CRLs). CSN exerts its function on E3 ligases by deconjugating the ubiquitin-related protein NEDD8 from the CRL cullin subunit. Thereby, CSN has an impact on multiple CRL-dependent processes. In recent years, advances have been made in understanding the structural organisation and biochemical function of CSN: Crystal structure analysis and mass spectrometry-assisted studies have come up with first models of the pair-wise and complex interactions of the 8 CSN subunits. Based on the analysis of mutant phenotypes, it can now be taken as an accepted fact that – at least in plants –the major biochemical function of CSN resides in its deneddylation activity, which is mediated by CSN subunit 5 (CSN5). Furthermore, it could be demonstrated that CSN function and deneddylation are required but not essential for CRL-mediated processes, and models for the role of neddylation and deneddylation in controlling CRL activity are emerging. Significant advances have also been made in identifying pathways that are growth restricting in the Arabidopsis csn mutants. Recently it has been shown that a G2 phase arrest, possibly due to genomic instability, restricts growth in Arabidopsis csn mutants. This review provides an update on recent advances in understanding CSN structure and function and summarises the current knowledge on its role in plant development and cell cycle progression.     

The role of GRAS proteins in plant signal transduction and development

GRAS proteins are a recently discovered family of plant-specific proteins named after GAI, RGA and SCR, the first three of its members isolated. Although the Arabidopsis genome encodes at least 33 GRAS protein family members only a few GRAS proteins have been characterized so far. However, it is becoming clear that GRAS proteins exert important roles in very diverse processes such as signal transduction, meristem maintenance and development. Here we present a survey of the different GRAS proteins and review the current knowledge of the function of individual members of this protein family.     

The role of protein kinases in the regulation of plant growth and development

We review the role of protein kinases in plant hormone-mediatedsignalling, nutrient signalling and cell cycle control and in the crosstalkbetween these different contributors to plant growth regulation. The areas ofhormone-mediated signalling covered include ABA-mediated responses to osmoticstress, wounding and pathogen attack, as well as ethylene and cytokininsignalling pathways. These areas involve members of several major protein kinasefamilies, including the SNFl-related protein kinase-2 (SnRK2) subfamily, thecalcium-dependent protein kinase (CDPK) family, the mitogen activated protein(MAP) kinase family, the glycogen synthase kinase (GSK)- 3/shaggy family and thereceptor-like protein kinase (RPK) family. In the section on nutrient signallingwe review the role of SnRK1 protein kinases in the global regulation of carbonmetabolism, including aspects of sugar sensing and assimilate partitioning, andwhat is known about nitrogen and sulphur nutrient signalling. In the cell cyclesection, we summarise progress in the elucidation of cell cycle control systemsin plants and discuss the interaction between cell cycle control anddevelopment. We expand further on the hypothesis of crosstalk between differentsignalling pathways in a separate section in which we discuss evidence forinteraction between plant growth regulators and the cell cycle, betweendifferent nutrient signalling pathways, between nutrient and cell cyclesignalling and between nutrient and ABA signalling.     

Concanavalin A-mediated agglutination of plant plastids

Cucumber (Cucumis sativus L.) and pear (Pyrus domestica Medik.) fruit proplastids, and pea (Pisum sativum L., cv. Meteor) leaf chloroplasts, extracted by osmotic rupture of protoplasts isolated after degradation of the cell walls by cellulase and pectinase, agglutinated in the presence of Con A. Agglutination of cucumber proplastids was inhibited by anti-Con A and by methyl D-gluco/manno pyranosides but not by methyl D-galactopyranoside. Fluorescein isothiocyanate-conjugated Con A (FITC-Con A) rendered agglutinated clumps fluorescent. If cellulase was omitted from the macerating medium, Con A-mediated agglutination did not occur even if proplatids were subsequently incubated with cellulase. Proplastids and chloroplasts extracted by conventional mechanical disruption methods were not agglutinated by Con A and did not acquire fluorescence with FITC-Con A. However, cucumber proplastids so extracted could be agglutinated by Con A if incubated with cellulase after preparation.Abbreviation Con A Concanavalin A (Jackbean phytohemagglutinin)     

The role of NAD biosynthesis in plant development and stress responses

Background

Pyridine nucleotides are essential for electron transport and serve as co-factors in multiple metabolic processes in all organisms. Each nucleotide has a particular role in metabolism. For instance, the NAD/NADP ratio is believed to be responsible for sustaining the functional status of plant cells. However, since enzymes involved in the synthesis and degradation of NAD and NADP have not been fully identified, the physiological functions of these co-enzymes in plant growth and development are largely unknown.

Scope

This Botanical Briefing covers progress in the developmental and stress-related roles of genes associated with NAD biosynthesis in plants. Special attention will be given to assessments of physiological impacts through the modulation of NAD and NADP biosynthesis.

Conclusions

The significance of NAD biosynthesis in plant development and NADP biosynthesis in plant stress tolerance is summarized in this Briefing. Further investigation of cells expressing a set of NAD biosynthetic genes would facilitate understanding of regulatory mechanisms by which plant cells maintain NAD homeostasis.Key words: NAD biosynthesis, nicotinate/nicotinamide mononucleotide adenylyltransferase (NMNAT), chloroplastic NADP biosynthesis, NAD kinase 2 (NADK2)