Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction

We tested whether a plant's life time seed production is increased by parasitization of herbivores in a tritrophic system, Arabidopsis thaliana (Brassicaceae) plants, Pieris rapae (Lepidoptera: Pieridae) caterpillars and the solitary endoparasitoid Cotesia rubecula (Hymenoptera: Braconidae). We established seed production for intact A. thaliana plants, plants that were mechanically damaged, plants fed upon by parasitized caterpillars and plants fed upon by unparasitized caterpillars. In the first experiment, with ecotype Landsberg (erecta mutant), herbivory by unparasitized P. rapae caterpillars resulted in a strongly reduced seed production compared to undamaged plants. In contrast, damage by P. rapae caterpillars that had been parasitized by C. rubecula did not result in a significant reduction in seed production. For the second experiment with the ecotype Columbia, the results were identical. Plants damaged by unparasitized caterpillars only produced seeds on regrown shoots. Seed production of plants that had been mechanically damaged was statistically similar to that of undamaged plants. Production of the first ripe siliques by plants fed upon by unparasitized caterpillars was delayed by 18–22 days for Landsberg and 9–10 days for Columbia. We conclude that parasitization of P. rapae by C. rubecula potentially confers a considerable fitness benefit for A. thaliana plants when compared to plants exposed to feeding damage by unparasitized P. rapae larvae. Plants that attract parasitoids and parasitoids that respond to herbivore-induced plant volatiles will both experience selective advantage, justifying the use of the term mutualism for this parasitoid-plant interaction. This type of mutualism is undoubtedly very common in nature.     

Phytohormones in algae

In various algal taxa, essentially all known phytohormones were detected in concentrations comparable with their content in higher plants. The occurrence of diverse free and conjugated hormone forms substantiates the functioning of the complex system of metabolism and activity regulation of these compounds. In most cases, the spectrum of biological activities of algal hormones corresponds to the functions of higher plant hormones. Some physiological and biochemical processes in algal cells and tissues are under the control of several phytohormones. All these facts permit a consideration of the algal hormonal system as a full-value regulatory system.     

Induction of callus and plant regeneration in Vicoa indica

Callus cultures were initiated from the stem and leaf explants of aseptically grown Vicoa indica. A simple method is described for plant regeneration from callus and the rapid multiplication of the plants thus obtained. Callus initiation was optimum in Gamborg B5 (B5) basal medium containing either 2.0 mg l^-1 naphthaleneacetic acid (NAA) with 0.2 mg l^-1 kinetin (Kn) or 2.0 mg l^-1 6-benzylaminopurine (BAP) with 0.2 mg l^-1 NAA. The calli initiated on B5 medium were able to proliferate on both Murashige and Skoog (MS) and B5 basal medium. Shoot primordia were obtained from greenish callus on passage to B5 basal medium containing 3.0 mg l^-1 BAP and 1.0 mg l^-1 Kn. On further subculture onto B5 medium containing 0.2 mg l^-1 Kn the shoot primordia developed into plantlets.     

Herbivory in a spider through exploitation of an ant–plant mutualism

Spiders are thought to be strict predators [1]. We describe a novel exception: Bagheera kiplingi, a Neotropical jumping spider (Salticidae) that exploits a well-studied ant–plant mutualism, is predominantly herbivorous. From behavioral field observations and stable-isotope analyses, we show that the main diet of this host-specific spider comprises specialized leaf tips (Beltian food bodies; Figure 1A) from Vachellia spp. ant-acacias (formerly Acacia spp.), structures traded for protection in the plant's coevolved mutualism with Pseudomyrmex spp. ants that inhabit its hollow thorns [2]. This is the first report of a spider that feeds primarily and deliberately on plants.     

The role of multiple partners in a digestive mutualism with a protocarnivorous plant

Background and aims

The protocarnivorous plant Paepalanthus bromelioides (Eriocaulaceae) is similar to bromeliads in that this plant has a rosette-like structure that allows rainwater to accumulate in leaf axils (i.e. phytotelmata). Although the rosettes of P. bromelioides are commonly inhabited by predators (e.g. spiders), their roots are wrapped by a cylindrical termite mound that grows beneath the rosette. In this study it is predicted that these plants can derive nutrients from recycling processes carried out by termites and from predation events that take place inside the rosette. It is also predicted that bacteria living in phytotelmata can accelerate nutrient cycling derived from predators.

Methods

The predictions were tested by surveying plants and animals, and also by performing field experiments in rocky fields from Serra do Cipó, Brazil, using natural abundance and enriched isotopes of ¹⁵N. Laboratory bioassays were also conducted to test proteolytic activities of bacteria from P. bromelioides rosettes.

Key Results

Analyses of ¹⁵N in natural nitrogen abundances showed that the isotopic signature of P. bromelioides is similar to that of carnivorous plants and higher than that of non-carnivorous plants in the study area. Linear mixing models showed that predatory activities on the rosettes (i.e. spider faeces and prey carcass) resulted in overall nitrogen contributions of 26·5 % (a top-down flux). Although nitrogen flux was not detected from termites to plants via decomposition of labelled cardboard, the data on ¹⁵N in natural nitrogen abundance indicated that 67 % of nitrogen from P. bromelioides is derived from termites (a bottom-up flux). Bacteria did not affect nutrient cycling or nitrogen uptake from prey carcasses and spider faeces.

Conclusions

The results suggest that P. bromelioides derive nitrogen from associated predators and termites, despite differences in nitrogen cycling velocities, which seem to have been higher in nitrogen derived from predators (leaves) than from termites (roots). This is the first study that demonstrates partitioning effects from multiple partners in a digestion-based mutualism. Despite most of the nitrogen being absorbed through their roots (via termites), P. bromelioides has all the attributes necessary to be considered as a carnivorous plant in the context of digestive mutualism.     

Plant glandular trichomes mediate protective mutualism in a spider–plant system

1. Although several species of Peucetia (Oxyopidae) live strictly in association with plants bearing glandular trichomes worldwide, to date little is known about whether these associations are mutualistic. 2. In this study we manipulated the presence of Peucetia flava on the glandular plant Rhynchanthera dichotoma in the rainy and post‐rain season, to test the strength of its effects on leaf, bud, and flower damage and plant reproductive output. In addition, we ran independent field experiments to examine whether these sticky structures improve spider fidelity to plants. 3. Peucetia suppressed some species of foliar phytophages, but not others. Although spiders have reduced levels of leaf herbivory, this phenomenon was temporally conditional, i.e. occurred only in the post‐rain but not in the rainy season. Floral herbivory was also reduced in the presence of spiders, but these predators did not affect plant fitness components. 4. Plants that had their glandular trichomes removed retained fewer insects than those bearing such structures. Spiders remained longer on plants with glandular trichomes than on plants in which these structures had been removed. Isotopic analyses showed that spiders that fed on live and dead labelled flies adhered to the glandular hairs in similar proportions. 5. Spiders incurred no costs to the plants, but can potentially increase individual plant fitness by reducing damage to reproductive tissues. Temporal conditionality probably occurred because plant productivity exceeded herbivore consumption, thus dampening top‐down effects. Specialisation to live on glandular plants may have favoured scavenging behaviour in Peucetia, possibly an adaptation to periods of food scarcity.     

Piriformospora indica affects plant growth by auxin production

Piriformospora indica has been shown to improve the growth of many plant species including Arabidopsis thaliana , but the mechanism by which this is achieved is still unclear. Arabidopsis root colonization by P. indica was examined in sterile culture on the medium of Murashige and Skoog. P. indica formed intracellular structures in Arabidopsis root epidermal cells and caused changes in root growth, leading to stunted and highly branched root systems. This effect was because of a diffusible factor and could be mimicked by IAA. In addition, P. indica was shown to produce IAA in liquid culture. We suggest that auxin production affecting root growth is responsible for, or at least contributes to, the beneficial effect of P. indica on its host plants.     

Piriformospora indica enhances plant growth by transferring phosphate

Piriformospora indica is an endophytic fungus that colonized monocot as well as dicot. P. indica has been termed as plant probiotic because of its plant growth promoting activity and its role in enhancement of the tolerance of the host plants against abiotic and biotic stresses. In our recent study, we have characterized a high affinity phosphate transporter (PiPT) and by using RNAi approach, we have demonstrated the involvement of PiPT in P transfer to the host plant. When knockdown strains of PiPT-P. indica was colonized with the host plant, it resulted in the impaired growth of the host plants. Here we have analyzed and discussed whether the growth promoting activity of P. indica is its intrinsic property or it is dependent on P availability. Our data explain the correlation between the availability of P and growth-promoting activity of P. indica.Key words: Piriformospora indica, phosphate transport, plant growth promotionPhosphorous (P) is one of the most essential mineral nutrients for plant growth and development. In the soil P is present mainly in the form of sparingly soluble complexes that are not directly accessible to plants. Thus, it is the nutrient that limits crop production throughout the world.¹ Plants have therefore evolved a range of strategies to increase the availability of soil P, which include both morphological and biochemical changes at the soil-root interface. For example, increased root growth and branching, proliferation of root hairs, and release of root exudates can increase plant access to inorganic phosphate (Pi) from otherwise poorly available sources.^2,3 Plant root possess two distinct modes of phosphate uptake, direct uptake by its own transporters and indirect uptake through mycorrhizal associations. In plants several high affinity P transporters specifically associated with the uptake of Pi from soil solution. Expression of these transporters is induced in response to P deficiency and enables Pi to be effectively taken up against the large concentration gradient that occurs between the soil solution and internal plant tissues.⁴ However, in arbuscular mycorrhizal associations (indirect uptake), plants acquire Pi from the extensive network of fine extra radical hyphae of fungus, that extend beyond root depletion zones to mine new regions of the soil.⁵ In the case of arbuscular mycorrhizal fungi (AMF), including Glomus versiforme and G. intraradices, the regulation of phosphate transporters that are expressed, typically upregulated under P deficiency but their role in P transfer to the host plant have not been characterized.^5,6P. indica was reported to be involved in high salt tolerance, disease resistance and strong growth-promoting activities leading to enhancement of host plant yield.^7–9 Recently, we have shown the role of PiPT in the P transport to the host plant.¹⁰ Here we discuss the performance of P. indica (grown under P-rich and -deprived conditions and colonized with the host plant) and its involvement in the P transportation to, and the growth of the host plant.     

Patterns of interaction between Populus Esch5 and Piriformospora indica: a transition from mutualism to antagonism

Piriformospora indica (Sebacinaceae, Basidiomycota) is an axenically cultivable, plant growth promoting root endophyte with a wide host range, including Populus. Rooting of Populus Esch5 explants started within 6 days after transfer to WPM medium. If such plantlets with roots were inoculated with P. indica, there was an increase in root biomass, and the number of 2nd order roots was increased significantly. A totally different observation was recorded when the explants were placed into WPM with pre-grown P. indica. The interaction led to complete blocking of root production and severely inhibited plant growth. Additionally, branched aerial roots appeared which did not penetrate the medium. On contact with the fungal colony or the medium, the ends of the aerial roots became inflated. Prolonged incubation stimulated the fungus to colonize aerial parts of the plant (stem and leaves). Mycelium not only spread on the surface of the aerial parts, but also invaded the cortical tissues inter- and intracellularly. Detached Populus leaves remained vital for 4 - 5 weeks on sterile agar media or on AspM medium with pre-grown P. indica. When the fungus was pre-grown on culture media such as WPM, containing ammonium as the main source of nitrogen, leaves in contact with the cultures turned brownish within 4 - 12 h. Thereafter, the leaves bleached, and about one day later had become whitish. Thus, cultural conditions could alter the behaviour of the fungus drastically: the outcome of the interaction between plant and fungus can be directed from mutualistic to antagonistic, characterized by fungal toxin formation and extension of the colonization to Populus shoots.     

Repetitive somatic embryogenesis and plant regeneration in Garcinia indica choiss

Summary Immature seeds of Garcinia indica Choiss, were exeised from immature fruits and cultured on Lloyd and McCown (1980), woody plant medium (WPM) with different combinations of auxins and cytokinins. Somatic embryos were obtained on the media supplemented with 6-benzy laminopurine (BA; 2.2–22.1 μM) alone or in combination with α-naphthalene acetic acid (NAA; 2.6 μM) with 80% frequency within a period of 2–3 wk. Subculture of embryos on medium containing BA (16.0 μM) supplemented with indole-3-acetic acid (IAA: 2.8–5.7 μM) and/or kinetin (4.6 μM) gave rise to clusters of secondary somatic embryos along with maturation of primary embryos. In subsequent subculture on hormone-free half-strength WPM, the embryo clusters germinated with an increase in the number of secondary somatic embryos. About 70% of somatic embryos germinated into complete plantlets, which were successfully established under greenhouse conditions.     

Seed dispersal by hornets: An unusual insect‐plant mutualism

Vespicochory, seed dispersal by hornets, is a rare seed dispersal mechanism in angiosperms and, to date, there are few records of this phenomenon.Through field investigations and behavioral assays conducted in four populations of Stemona tuberosa from 2011–2016, we demonstrate that hornets are the primary seed dispersers of S. tuberosa and play an important role in long-distance seed dispersal in this species. Furthermore, some ant species act as secondary dispersers and may transport the seeds to safe sites.Hornets and ants provide complementary seed dispersal at different spatial scales. This unique example of insect-plant mutualism may be an underestimated but important strategy to ensure long-distance seed dispersal in other myrmecochorous plants.     

Florivore impacts on plant reproductive success and pollinator mortality in an obligate pollination mutualism

Florivores are present in many pollination systems and can have direct and indirect effects on both plants and pollinators. Although the impact of florivores are commonly examined in facultative pollination mutualisms, their effects on obligate mutualism remain relatively unstudied. Here, we used experimental manipulations and surveys of naturally occurring plants to assess the effect of florivory on the obligate pollination mutualism between yuccas and yucca moths. Yucca filamentosa (Agavaceae) is pollinated by the moth Tegeticula cassandra (Lepidoptera: Prodoxidae), and the mutualism also attracts two florivores: a generalist, the leaf-footed bug Leptoglossus phyllopus (Hemiptera: Coreidae), and a specialist, the beetle Hymenorus densus (Coleoptera: Tenebrionidae). Experimental manipulations of leaf-footed bug densities on side branches of Y. filamentosa inflorescences demonstrated that feeding causes floral abscission but does not reduce pollen or seed production in the remaining flowers. Similar to the leaf-footed bugs, experimental manipulations of beetle densities within individual flowers demonstrated that beetle feeding also causes floral abscission, but, in addition, the beetles also cause a significant reduction in pollen availability. Path analyses of phenotypic selection based on surveys of naturally occurring plants revealed temporal variation in the plant traits important to plant fitness and the effects of the florivores on fitness. Leaf-footed bugs negatively impacted fitness when fewer plants were flowering and leaf-footed bug density was high, whereas beetles had a positive effect on fitness when there were many plants flowering and their densities were low. This positive effect was likely due to adult beetles consuming yucca moth eggs while having a negligible effect on floral abscission. Together, the actions of both florivores either augmented the relationship of plant traits and fitness or slightly weakened the relationship. Overall, the results suggest that, although florivores are always present during flowering, the impact of florivores on phenotypic selection in yuccas is strongly mitigated by changes in their densities on plants from year to year. In contrast, both florivores consistently influenced pollinator larval mortality through floral abscission, and H. densus beetles additionally via the consumption of pollinator eggs.     

A facultative mutualism between aphids and an invasive ant increases plant reproduction

1. The consequences to plants of ant–aphid mutualisms, particularly those involving invasive ants, are poorly studied. Ant–aphid mutualisms may increase or decrease plant fitness depending on the relative cost of herbivory by ant‐tended aphids versus the relative benefit of increased ant suppression of other (non‐aphid) herbivores. 2. We conducted field and greenhouse experiments in which we manipulated the presence and absence of cotton aphids (Aphis gossypii) on cotton plants to test the hypothesis that a mutualism between cotton aphids and an invasive ant, the red imported fire ant (Solenopsis invicta), benefits cotton plants by increasing fire ant suppression of caterpillars. We also manipulated caterpillar abundance to test whether the benefit of the mutualism varied with caterpillar density. 3. We found that more fire ants foraged on plants with cotton aphids than on plants without cotton aphids, which resulted in a significant reduction in caterpillar survival and caterpillar herbivory of leaves, flower buds, and bolls on plants with aphids. Consequently, cotton aphids indirectly increased cotton reproduction: plants with cotton aphids produced 16% more bolls, 25% more seeds, and 10% greater seedcotton mass than plants without aphids. The indirect benefit of cotton aphids, however, varied with caterpillar density: the number of bolls per plant at harvest was 32% greater on plants with aphids than on plants without aphids at high caterpillar density, versus just 3% greater at low caterpillar density. 4. Our results highlight the potential benefit to plants that host ant–hemipteran mutualisms and provide the first experimental evidence that the consequences to plants of an ant–aphid mutualism vary at different densities of non‐aphid herbivores.     

Phytohormones and Cytoskeleton

Various aspects of the interaction between phytohormones and principal components of the cytoskeleton are considered. Four levels of this interaction are discussed: (1) the spatial organization of microtubules and microfilaments; (2) the synthesis and modification of cytoskeletal proteins; (3) the cytoskeleton involvement in processes, which are under hormonal control; and (4) the cytoskeleton involvement in phytohormone functioning.     

Infiltration of a facultative ant–plant mutualism by the introduced Argentine ant: effects on mutualist diversity and mutualism benefits

1. Ant–plant mutualisms have been the focus of considerable empirical research, but few studies have investigated how introduced ants affect these interactions. Using 2 years of survey data, this study examines how the introduced Argentine ant [Linepithema humile (Mayr)] differs from native ants with respect to its ability to protect the extrafloral nectary‐bearing coast barrel cactus (Ferocactus viridescens) in Southern California. 2. Eighteen native ant species visited cacti in uninvaded areas, but cacti in invaded areas were primarily visited by the Argentine ant. The main herbivore of the coast barrel cactus present at the study sites is a leaf‐footed bug (Narnia wilsoni). 3. Herbivore presence (the fraction of surveys in which leaf‐footed bugs were present on individual cacti) was negatively related to ant presence (the fraction of surveys in which ants were present on individual cacti). Compared with cacti in uninvaded areas, those in invaded areas were less likely to have herbivores and when they did had them less often. 4. Seed mass was negatively related to herbivore presence, and this relationship did not differ for cacti in invaded areas versus those in uninvaded areas. 5. Although the Argentine ant might provide superior protection from herbivores, invasion‐induced reductions in ant mutualist diversity could potentially compromise plant reproduction. The cumulative number of ant species on individual cacti over time was lower in invaded areas and was associated with a shortened seasonal duration of ant protection and reduced seed mass. These results support the hypothesis that multiple partners may enhance mutualism benefits.     

Intraguild mutualism

Although studies of species linked by a common resource (i.e. ecological guilds) have so far mainly focused on competition and predation, guilds are also good places to find mutualism. In this review we consider some three- and four-species community modules to illustrate examples of wide relevance. Mutualism arises from various direct and indirect trophic and non-trophic interactions between species--and within modules both with and without intraguild predation. Species removal and augmentation experiments, other manipulations, direct measurements, and path-analytic methods can determine the presence and intensity of mutualism within guilds. Such studies, particularly when associated with existing theory and new theoretical development, can help advance an interaction-based approach to community analysis that recognizes linkages among mutualism, predation and competition in natural systems.