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From seed to seed: the role of photoreceptors in Arabidopsis development.

As sessile organisms, plants have evolved a multitude of developmental responses to cope with the ever-changing environmental conditions that challenge the plant throughout its life cycle. Of the many environmental cues that regulate plant development, light is probably the most important. From determining the developmental pattern of the emerging seedling, to influencing the organization of organelles to best maximize energy available for photosynthesis, light has dramatic effects on development during all stages of plant life. In plants, three classes of photoreceptors that mediate light perception have been characterized at the molecular level. The phytochromes recognize light in the red portion of the spectrum, while cryptochromes and phototropins perceive blue and UVA light. In this review, we discuss the different aspects of development that are regulated by these photoreceptors in the model plant species Arabidopsis thaliana and how the phytochromes, cryptochromes, and phototropins bring about changes in development seen in the growing plant.

Arabidopsis↗

Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development.

Plant cells employ the actin cytoskeleton to stably position organelles, as tracks for long distance transport, and to reorganize the cytoplasm in response to developmental and environmental cues. While diverse classes of actin binding proteins have been implicated in growth control, the mechanisms of cytoskeletal reorganization and the cellular functions of specific actin filament arrays are unclear. Arabidopsis trichome morphogenesis includes distinct requirements for the microtubule and actin filament cytoskeletons. It also is a genetically tractable process that is providing new knowledge about cytoskeleton function in plants. The "distorted group" of mutants defines a class of at least eight genes that are required during the actin-dependent phase of trichome growth. Using map-based cloning and a candidate gene approach, we identified mutations in ARP3 (ATARP3) and ARP2 (ATARP2) genes as the cause of the distorted1 (dis1) and wurm (wrm) phenotypes, respectively. ARP2 and ARP3 are components of the evolutionarily conserved ARP2/3 complex that nucleates actin filament polymerization [3]. Mutations in DIS1 and WRM caused severe trichome growth defects but had relatively mild effects on shoot development. DIS1 rescued the phenotype of Deltaarp3 when overexpressed in S. cerevisiae. Developing dis1 trichomes had defects in cytoplasmic actin bundle organization and reduced relative amounts of cytoplasmic actin filaments in developing branches.

Actin Cytoskeleton↗

Lipoxygenase is involved in the control of potato tuber development.

Plant lipoxygenases (LOXs) are a functionally diverse class of dioxygenases implicated in physiological processes such as growth, senescence, and stress-related responses. LOXs incorporate oxygen into their fatty acid substrates and produce hydroperoxide fatty acids that are precursors of jasmonic acid and related compounds. Here, we report the involvement of the tuber-associated LOXs, designated the Lox1 class, in the control of tuber growth. RNA hybridization analysis showed that the accumulation of Lox1 class transcripts was restricted to developing tubers, stolons, and roots and that mRNA accumulation correlated positively with tuber initiation and growth. In situ hybridization showed that Lox1 class transcripts accumulated in the apical and subapical regions of the newly formed tuber, specifically in the vascular tissue of the perimedullary region, the site of the most active cell growth during tuber enlargement. Suppression mutants produced by expressing antisense coding sequence of a specific tuber LOX, designated POTLX-1, exhibited a significant reduction in LOX activity in stolons and tubers. The suppression of LOX activity correlated with reduced tuber yield, decreased average tuber size, and a disruption of tuber formation. Our results indicate that the pathway initiated by the expression of the Lox1 class genes of potato is involved in the regulation of tuber enlargement.

Cell Division↗

Dual temporal role of plastid sigma factor 6 in Arabidopsis development.

Plants contain nuclear-coded sigma factors for initiation of chloroplast transcription. The in vivo function of individual members of the sigma gene family has become increasingly accessible by knockout and complementation strategies. Here we have investigated plastid gene expression in an Arabidopsis (Arabidopsis thaliana) mutant with a defective gene for sigma factor 6. RNA gel-blot hybridization and real-time reverse transcription polymerase chain reaction together indicate that this factor has a dual developmental role, with both early and persistent (long-term) activities. The early role is evident from the sharp decrease of certain plastid transcripts only in young mutant seedlings. The second (persistent) role is reflected by the up- and down-regulation of other transcripts at the time of primary leaf formation and subsequent vegetative development. We conclude that sigma 6 does not represent a general factor, but seems to have specialized roles in developmental stage- and gene-specific plastid transcription. The possibility that plastid DNA copy number might be responsible for the altered transcript patterns in mutant versus wild type was excluded by the results of DNA gel-blot hybridization. Retransformation of the knockout line with the full-length sigma 6 cDNA further established a causal relationship between the functional sigma gene and the resulting phenotype.

Arabidopsis↗

Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development.

Plants have evolved complex strategies to maintain phosphate (Pi) homeostasis and to maximize Pi acquisition when the macronutrient is limiting. Adjustment of root system architecture via changes in meristem initiation and activity is integral to the acclimation process. However, the mechanisms that monitor external Pi status and interpret the nutritional signal remain to be elucidated. Here, we present evidence that the Pi deficiency response, pdr2, mutation disrupts local Pi sensing. The sensitivity and amplitude of metabolic Pi-starvation responses, such as Pi-responsive gene expression or accumulation of anthocyanins and starch, are enhanced in pdr2 seedlings. However, the most conspicuous alteration of pdr2 is a conditional short-root phenotype that is specific for Pi deficiency and caused by selective inhibition of root cell division followed by cell death below a threshold concentration of about 0.1 mm external Pi. Measurements of general Pi uptake and of total phosphorus (P) in root tips exclude a defect in high-affinity Pi acquisition. Rescue of root meristem activity in Pi-starved pdr2 by phosphite (Phi), a non-metabolizable Pi analog, and divided-root experiments suggest that pdr2 disrupts sensing of low external Pi availability. Thus, PDR2 is proposed to function at a Pi-sensitive checkpoint in root development, which monitors environmental Pi status, maintains and fine-tunes meristematic activity, and finally adjusts root system architecture to maximize Pi acquisition.

Arabidopsis↗

Phytochrome A and Phytochrome B Have Overlapping but Distinct Functions in Arabidopsis Development.

Plant responses to red and far-red light are mediated by a family of photoreceptors called phytochromes. In Arabidopsis thaliana, there are genes encoding at least five phytochromes, and it is of interest to learn if the different phytochromes have overlapping or distinct functions. To address this question for two of the phytochromes in Arabidopsis, we have compared light responses of the wild type with those of a phyA null mutant, a phyB null mutant, and a phyA phyB double mutant. We have found that both phyA and phyB mutants have a deficiency in germination, the phyA mutant in far-red light and the phyB mutant in the dark. Furthermore, the germination defect caused by the phyA mutation in far- red light could be suppressed by a phyB mutation, suggesting that phytochrome B (PHYB) can have an inhibitory as well as a stimulatory effect on germination. In red light, the phyA phyB double mutant, but neither single mutant, had poorly developed cotyledons, as well as reduced red-light induction of CAB gene expression and potentiation of chlorophyll induction. The phyA mutant was deficient in sensing a flowering response inductive photoperiod, suggesting that PHYA participates in sensing daylength. In contrast, the phyB mutant flowered earlier than the wild type (and the phyA mutant) under all photoperiods tested, but responded to an inductive photoperiod. Thus, PHYA and PHYB appear to have complementary functions in controlling germination, seedling development, and flowering. We discuss the implications of these results for possible mechanisms of PHYA and PHYB signal transduction.

Journal Article↗

Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar.

Sugars have signaling roles in a wide variety of developmental processes in plants. To elucidate the regulatory components that constitute the glucose signaling network governing plant growth and development, we have isolated and characterized two Arabidopsis glucose insensitive mutants, gin5 and gin6, based on a glucose-induced developmental arrest during early seedling morphogenesis. The T-DNA-tagged gin6 mutant abrogates the glucose-induced expression of a putative transcription factor, ABI4, previously shown to be involved in seed-specific abscisic acid (ABA) responses. Thus, ABI4 might be a regulator involved in both glucose- and seed-specific ABA signaling. The characterization of the gin5 mutant, on the other hand, reveals that glucose-specific accumulation of ABA is essential for hexokinase-mediated glucose responses. Consistent with this result, we show that three ABA-deficient mutants (aba1-1, aba2-1, and aba3-2) are also glucose insensitive. Exogenous ABA can restore normal glucose responses in gin5 and aba mutants but not in gin6 plants. Surprisingly, only abi4 and abi5-1 but not other ABA-insensitive signaling mutants (abi1-1, abi2-1, and abi3-1) exhibit glucose insensitivity, indicating the involvement of a distinct ABA signaling pathway in glucose responses. These results provide the first direct evidence to support a novel and central role of ABA in plant glucose responses mediated through glucose regulation of both ABA levels by GIN5 and ABA signaling by GIN6/ABI4.

Abscisic Acid↗

N-glycoprotein biosynthesis in plants: recent developments and future trends.

N-glycosylation is a major modification of proteins in plant cells. This process starts in the endoplasmic reticulum by the co-translational transfer of a precursor oligosaccharide to specific asparagine residues of the nascent polypeptide chain. Processing of this oligosaccharide into high-mannose-type, paucimannosidic-type, hybrid-type or complex-type N-glycans occurs in the secretory pathway as the glycoprotein moves from the endoplasmic reticulum to its final destination. At the end of their maturation, some plant N-glycans have typical structures that differ from those found in their mammalian counterpart by the absence of sialic acid and the presence of beta(1,2)-xylose and alpha( 1,3)-fucose residues. Glycosidases and glycosyltransferases that respectively catalyse the stepwise trimming and addition of sugar residues are generally considered as working in a co-ordinated and highly ordered fashion to form mature N-glycans. On the basis of this assembly line concept, fast progress is currently made by using N-linked glycan structures as milestones of the intracellular transport of proteins along the plant secretory pathway. Further developments of this approach will need to more precisely define the topological distribution of glycosyltransferases within a plant Golgi stack. In contrast with their acknowledged role in the targeting of lysosomal hydrolases in mammalian cells, N-glycans have no specific function in the transport of glycoproteins into the plant vacuole. However, the presence of N-glycans, regardless of their structures, is necessary for an efficient secretion of plant glycoproteins. In the biotechnology field, transgenic plants are rapidly emerging as an important system for the production of recombinant glycoproteins intended for therapeutic purposes, which is a strong motivation to speed up research in plant glycobiology. In this regard, the potential and limits of plant cells as a factory for the production of mammalian glycoproteins will be illustrated.

Animals↗

Ethylene production throughout growth and development of plants.

Ethylene production by 10 or 20 m2 stands of wheat, soybean, lettuce, potato, and tomato was monitored throughout growth and development in an atmospherically closed plant chamber. Chamber ethylene levels varied among species and rose during periods of canopy expansion and rapid growth for all species. Following this, ethylene levels either declined during seed fill and maturation for wheat and soybean, or remained relatively constant for potato and tomato (during flowering and early fruit development). Lettuce plants were harvested during rapid growth and peak ethylene production. Chamber ethylene levels increased rapidly during tomato ripening, reaching concentrations about 10 times that measured during vegetative growth. The highest ethylene production rates during vegetative growth ranged from 1.6 to 2.5 nmol m-2 d-1 during rapid growth of lettuce and wheat stands, or about 0.3 to 0.5 nmol g-1 fresh weight per hour. Estimates of stand ethylene production during tomato ripening showed that rates reached 43 nmol m-2 d-1 in one study and 93 nmol m-2 d-1 in a second study with higher lighting, or about 50x that of the rate during vegetative growth of tomato. In a related test with potato, the photoperiod was extended from 12 to 24 hours (continuous light) at 58 days after planting (to increase tuber yield), but this change in the environment caused a sharp increase in ethylene production from the basal rate of 0.4 to 6.2 nmol m-2 d-1. Following this, the photoperiod was changed back to 12 h at 61 days and ethylene levels decreased. The results suggest three separate categories of ethylene production were observed with whole stands of plants: 1) production during rapid vegetative growth, 2) production during climacteric fruit ripening, and 3) production from environmental stress.

Biomass↗

Signalling in light-controlled development.

Plants continuously analyze the nature of environmental light signals using an array of at least eight informational photoreceptors, each with differential functional roles. Molecular and genetic studies are identifying an increasing assembly of potential or established signalling intermediates involved in transducing perceived signals from these photoreceptors to photoresponsive genes. The emerging picture suggests a complex network with both separate and shared early signalling pathway segments which appear to converge to regulate developmentally important genes through a set of master regulators.

Light↗

Use of red fluorescent protein from Discosoma sp. (dsRED) as a reporter for plant gene expression.

The suitability of the recently described red fluorescent protein dsRED from reef corals for use as a reporter in plant molecular biology was investigated. Based on the clone pDSRED (Clontech), plant expression vectors were constructed for constitutive dsRED expression in the cytosol, the endoplasmic reticulum and the vacuole. Fluorescence microscopy of tobacco BY2 suspension culture cells transiently expressing the plant vectors generated proved that cytosolic expression of the dsRED gives rise to readily detectable levels of red fluorescence, whereas expression in the ER was poor. Vacuolar dsRED expression did not result in any significant fluorescence. dsRED transgenic tobacco SR1 plants were generated to test the sensitivity of dsRED as a reporter in an autofluorescent background, and to identify the possible impact of the introduced fluorescent protein on morphogenesis, plant development and fertility. During the transformation and regeneration phase plants did not show any abnormalities, indicating that dsRED is not interfering with plant development and morphogenesis. Regenerated plants were analysed by PCR, Western blot and fluorescence microscopy for the presence and expression of the transferred genes. The filter sets chosen for fluorescence microscopy proved to be able to block the red chlorophyll fluorescence completely, allowing specific dsRED detection. Best expression levels were obtained with dsRED targeted to the cytosol or chloroplasts. ER-targeted expression of dsRED also gave rise to readily detectable fluorescence levels, whereas vacuolar expression yielded no fluorescence. dsRED transgenic plant lines expressing the protein in the cytosol, ER or chloroplast proved to be fertile. Seed set and germination were normal, except that the seeds and seedlings maintained the red fluorescence phenotype.

Animals↗

Sorption of ozone by 'New Yorker' tomato leaves.

Tomato (Lycopersicon esculentum Mill.) 'New Yorker' plants were exposed to O(3) to compare leaf diffusive conductance (LDC) before exposure to O(3) with O(3) sorption rates and visible injury ratings. Two plant development stages and four or five leaf growth stages were examined. The LDC varied among leaf growth stages and between plant development stages and leaf surfaces; there was no continuity in the LDC pattern. Sorption rates differed among some leaf growth stages, and between plant development stages in expanding leaves (growth stage 1). For both development stages high sorption rates occurred in fully mature leaves; otherwise little similarity between corresponding leaf growth stages was evident. Total O(3) flux to the leaf was not well predicted by the LDC for water vapour; nor was visible injury well related to total flux. Differential mesophyll processes and leaf surface sorption capabilities may have accounted for some of the inconsistencies observed.

Journal Article↗

Plant reproductive development during spaceflight.

Reproductive development in microgravity has now been studied in a variety of plants; Arabidopsis, Brassica, and Triticum have been especially well studied. Earlier indications that gravity might be required for some stage of reproductive development have now been refuted. Nevertheless, the spaceflight environment presents many unique challenges that have often compromised the ability of plants to reproduce. These include limitations in hardware design to compensate for the unique environmental characteristics of microgravity, especially absence of convective air movement. Pollen development has been shown to be sensitive to high concentrations of ethylene prevailing on various orbital platforms. Barring these gross environmental problems, androecium and gynoecium development occur normally in microgravity, in that functional propagules are produced. Nonetheless, qualitative changes in anther and pistil development have been shown, and significant qualitative changes occur in storage reserve deposition during seed development. Apart from the intrinsic biological importance of these results, consequences of diminished seed quality when plants are grown in the absence of gravity will detract from the utility of plant-based life support systems. By understanding gravity's role in determining the microenvironments that prevail during reproductive development, counter-measures to these obstacles can be found, while at the same time providing basic knowledge that will have broader agricultural significance.

Fruit↗

Arabidopsis E2Fa plays a bimodal role in regulating cell division and cell growth.

The onset of cell cycle in mammalian systems is primarily controlled by E2F-like transcription factors. Recent evidence shows that plant E2F homologs and their associated proteins likely play similar roles in higher plant development. We studied the function of plant E2F in gene regulation and morphogenesis using transgenic Arabidopsis plants over-expressing AtE2Fa. Examination of rosettes showed that AtE2Fa over-expression resulted in increased expression of both cell cycle promoters and cell cycle inhibitors. The positive factors up-regulated by AtE2Fa emcompassed genes for G1/S transition, DNA synthesis and mitosis, and the negative factors up-regulated by AtE2Fa included RB1 , encoding the E2F binding protein, as well as KRP3 and KRP5 , encoding the plant CDK inhibitors. Moreover, AtE2Fa over-expression in rosettes led to elevated expression of ATPK19 , the homolog of the highly conserved S6 kinase that is known to enhance cell growth. The transgenic plants exhibited narrower rosette leaves when compared to wild-type control. Consistent with elevated expression of cell cycle inhibitors and ATPK19 , the mature rosette leaves displayed reduced cell number but increased cell size. These results demonstrate that AtE2Fa controls cell division and plant development by assuming a bimodal function in balancing the expression of both positive and negative regulators involved in cell division and growth.

Animals↗

Age- and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control.

Woody plants exhibit significant and predictable patterns of change in morphology and physiology as they become older and larger. Four models of potential pathways controlling these changes are presented: a stimulus-response model in which fully developed organs respond to changes in environment (defined here as everything external to the organ); an extrinsic model in which the attributes of developing organs are determined by environmental factors; an intrinsic model in which changes are a result of programmed changes in gene expression; and an extrinsic-intrinsic model in which changes in gene expression are induced by environmental factors. We review evidence that a genetic component is involved in controlling age- and size-related changes in foliar morphology and physiology and discuss the possibility of complex interactions among model pathways.

Models, Biological↗

Control of plant trichome development by a cotton fiber MYB gene.

Cotton (Gossypium spp) plants produce seed trichomes (cotton fibers) that are an important commodity worldwide; however, genes controlling cotton fiber development have not been characterized. In Arabidopsis thaliana the MYB gene GLABRA1 (GL1) is a central regulator of trichome development. Here, we show that promoter of a cotton fiber gene, RD22-like1 (RDL1), contains a homeodomain binding L1 box and a MYB binding motif that confer trichome-specific expression in Arabidopsis. A cotton MYB protein GaMYB2/Fiber Factor 1 transactivated the RDL1 promoter both in yeast and in planta. Real-time PCR and in situ analysis showed that GaMYB2 is predominantly expressed early in developing cotton fibers. After transferring into Arabidopsis, GL1::GaMYB2 rescued trichome formation of a gl1 mutant, and interestingly, 35S::GaMYB2 induced seed-trichome production. We further demonstrate that the first intron of both GL1 and GaMYB2 plays a role in patterning trichomes: it acts as an enhancer in trichome and a repressor in nontrichome cells, generating a trichome-specific pattern of MYB gene expression. Disruption of a MYB motif conserved in intron 1 of GL1, WEREWOLF, and GaMYB2 genes affected trichome production. These results suggest that cotton and Arabidopsis use similar transcription factors for regulating trichomes and that GaMYB2 may be a key regulator of cotton fiber development.

Amino Acid Motifs↗

Plant growth, development and embryogenesis during Salyut-7 flight.

The growth and geotropic movements of roots and hypocotyls of lettuce have been studied on board the Salyut 7 station in a stationary position and on the centrifuge at 0.01, 0.1 and 1 g. On the centrifuge at 0.1 and 0.01 g as well as under weightlessness, the final length of hypocotyls was by 8-16% greater than in control plants on the centrifuge at 1 g. The length of roots, however, was reduced by 17% at 0.01 g and under weightlessness; at 0.1 g their growth is much the same as at 1 g. On the Earth, while growing in a vertical position, and in space at 0 < or = g, the roots and hypocotyls deviate from the longitudinal axis of the seed. Average values of deviation eagles on the Earth are always equal to zero, while this is not always the case in space, which indicates the biological effect of microgravity conditions on board a spacecraft. The threshold of geotropic sensitiveness of lettuce hypocotyls, calculated from the linear regression parameters of the dependence of the response geotropic reaction upon the value of the centrifugal force, comprised 2.9 x 10(-3) g. In the Fiton 3 micro-greenhouse under spaceflight conditions, the plants of Arabidopsis thaliana (L) Heynh have, for the first time, undergone a full cycle of individual development. The seeds sown during the flight germinated, performed growth processes, formed vegetative and generative organs and, judging by the final result, they succeeded in fecundation, embryogenesis and ripening. Despite the noted modification of growth and development of plants in space, 42% of formed seeds appeared to be valuable biologically.

Arabidopsis↗