Herbivorous insects use diverse feeding strategies to obtain nutrients from their host plants. Rather than acting as passive victims in these interactions, plants respond to herbivory with the production of toxins and defensive proteins that target physiological processes in the insect. Herbivore-challenged plants also emit volatiles that attract insect predators and bolster resistance to future threats. This highly dynamic form of immunity is initiated by the recognition of insect oral secretions and signals from injured plant cells. These initial cues are transmitted within the plant by signal transduction pathways that include calcium ion fluxes, phosphorylation cascades, and, in particular, the jasmonate pathway, which plays a central and conserved role in promoting resistance to a broad spectrum of insects. A detailed understanding of plant immunity to arthropod herbivores will provide new insights into basic mechanisms of chemical communication and plant-animal coevolution and may also facilitate new approaches to crop protection and improvement.

Plant Immunity to Insect Herbivores

Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany

Plants respond to herbivory through various morphological, biochemicals, and molecular mechanisms to counter/offset the effects of herbivore attack. The biochemical mechanisms of defense against the herbivores are wide-ranging, highly dynamic, and are mediated both by direct and indirect defenses. The defensive compounds are either produced constitutively or in response to plant damage, and affect feeding, growth, and survival of herbivores. In addition, plants also release volatile organic compounds that attract the natural enemies of the herbivores. These strategies either act independently or in conjunction with each other. However, our understanding of these defensive mechanisms is still limited. Induced resistance could be exploited as an important tool for the pest management to minimize the amounts of insecticides used for pest control. Host plant resistance to insects, particularly, induced resistance, can also be manipulated with the use of chemical elicitors of secondary metabolites, which confer resistance to insects. By understanding the mechanisms of induced resistance, we can predict the herbivores that are likely to be affected by induced responses. The elicitors of induced responses can be sprayed on crop plants to build up the natural defense system against damage caused by herbivores. The induced responses can also be engineered genetically, so that the defensive compounds are constitutively produced in plants against are challenged by the herbivory. Induced resistance can be exploited for developing crop cultivars, which readily produce the inducible response upon mild infestation, and can act as one of components of integrated pest management for sustainable crop production.

https://www.tandfonline.com/doi/pdf/10.4161/psb.21663

Mechanisms of plant defense against insect herbivores

Plants have evolved a plethora of different chemical defenses covering nearly all classes of (secondary) metabolites that represent a major barrier to herbivory: Some are constitutive; others are induced after attack. Many compounds act directly on the herbivore, whereas others act indirectly via the attraction of organisms from other trophic levels that, in turn, protect the plant. An enormous diversity of plant (bio)chemicals are toxic, repellent, or antinutritive for herbivores of all types. Examples include cyanogenic glycosides, glucosinolates, alkaloids, and terpenoids; others are macromolecules and comprise latex or proteinase inhibitors. Their modes of action include membrane disruption, inhibition of nutrient and ion transport, inhibition of signal transduction processes, inhibition of metabolism, or disruption of the hormonal control of physiological processes. Recognizing the herbivore challenge and precise timing of plant activities as well as the adaptive modulation of the plants’ metabolism is important so that metabolites and energy may be efficiently allocated to defensive activities.

Plant Defense Against Herbivores: Chemical Aspects

https://www.cell.com/molecular-plant/pdf/S1674-2052(14)60932-1.pdf

Growth-defense tradeoffs in plants: a balancing act to optimize fitness.

Plants produce metabolites that directly decrease herbivore performance, and as a consequence, herbivores are selected for resistance to these metabolites. To determine whether these metabolites actually function as defenses requires measuring the performance of plants that are altered only in the production of a certain metabolite. To date, the defensive value of most plant resistance traits has not been demonstrated in nature. We transformed native tobacco(Nicotiana attenuata) with a consensus fragment of its two putrescine N-methyl transferase (pmt) genes in either antisense or inverted-repeat (IRpmt) orientations. Only the latter reduced (by greater than 95%) constitutive and inducible nicotine. With D4-nicotinic acid (NA), we demonstrate that silencing pmt inhibits nicotine production, while the excess NA dimerizes to form anatabine. Larvae of the nicotine-adapted herbivore Manduca sexta (tobacco hornworm) grew faster and, like the beetle Diabrotica undecimpunctata, preferred IRpmt plants in choice tests. When planted in their native habitat, IRpmt plants were attacked more frequently and, compared to wild-type plants, lost 3-fold more leaf area from a variety of native herbivores, of which the beet armyworm, Spodoptera exigua, and Trimerotropis spp. grasshoppers caused the most damage. These results provide strong evidence that nicotine functions as an efficient defense in nature and highlights the value of transgenic techniques for ecological research.

/pdf/nicotine-s-defensive-function-in-nature-2uxrz9yhis.pdf

Nicotine's defensive function in nature.

Plants use many means to attract pollinators, including visual cues and odor. We investigated how nonpigment floral chemistry influences nectar removal, floral visitation, florivory, rates of outcrossing, and fitness through both male and female functions. We blocked expression of biosynthetic genes of the dominant floral attractant [benzyl acetone (Nachal1)] and nectar repellent [nicotine (Napmt1/2)] in all combinations in the native tobacco Nicotiana attenuata and measured their effects on plants in their native habitat. Both repellent and attractant were required to maximize capsule production and seed siring in emasculated flowers and flower visitation by native pollinators, whereas nicotine reduced florivory and nectar robbing.

https://science.sciencemag.org/content/sci/321/5893/1200.full.pdf

Field experiments with transformed plants reveal the sense of floral scents

Research into the genetic basis of the ecological sophistication of plants is hampered by the availability of transformable systems with a wealth of well-described ecological interactions. We present an Agrobacterium-mediated transformation system for the model ecological expression system, Nicotiana attenuata, a native tobacco that occupies the post-fire niche in the Great Basin Desert of North America. We describe a transformation vector and a transformation procedure that differs from the standard cultivated tobacco transformation protocols in its use of selectable markers, explants, media and cultivation conditions. We illustrate its utility in the transformations with genes coding for key enzymes in the oxylipin cascade (lipoxygenase, allene oxide synthase, hydroperoxide lyase) in antisense orientations and present high-throughput screens useful for the detection of altered phenotypes for the oxylipin cascade (green leaf volatiles and jasmonic acid after wounding).

Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system

Although nectar is known to be important, for example in plant–insect interactions, little has been known about the mechanism of its secretion; sucrose phosphate synthases are now reported to be essential for the synthesis of the sucrose component of nectar and the transporter protein SWEET9 is shown to mediate sucrose export into the extracellular space of the nectary. Nectar is an important factor in interactions between plants and insects, mediating both pollination and defensive mutualisms. The function and composition of floral nectaries have been well characterized, but the mechanism of nectar secretion has remained elusive. In a study of three flowering plant species, Wolf Frommer and colleagues show that sucrose phosphate synthases are highly expressed in floral nectaries and are essential for the synthesis of the sucrose component of nectar. The transporter protein SWEET9 mediates sucrose export from the site of production, in the nectary parenchyma, to the extracellular space of the nectary. Angiosperms developed floral nectaries that reward pollinating insects1. Although nectar function and composition have been characterized, the mechanism of nectar secretion has remained unclear2. Here we identify SWEET9 as a nectary-specific sugar transporter in three eudicot species: Arabidopsis thaliana, Brassica rapa (extrastaminal nectaries) and Nicotiana attenuata (gynoecial nectaries). We show that SWEET9 is essential for nectar production and can function as an efflux transporter. We also show that sucrose phosphate synthase genes, encoding key enzymes for sucrose biosynthesis, are highly expressed in nectaries and that their expression is also essential for nectar secretion. Together these data are consistent with a model in which sucrose is synthesized in the nectary parenchyma and subsequently secreted into the extracellular space via SWEET9, where sucrose is hydrolysed by an apoplasmic invertase to produce a mixture of sucrose, glucose and fructose. The recruitment of SWEET9 for sucrose export may have been a key innovation, and could have coincided with the evolution of core eudicots and contributed to the evolution of nectar secretion to reward pollinators.

Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9

Evidence for the in planta defensive function of trypsin protease inhibitors (TPIs) comes from observations of enhanced herbivore resistance after heterologous TPI expression or the manipulation of signal cascades that activate numerous defense responses, including TPI production; no studies have altered the expression of an endogenous pi gene to examine defensive function. We isolated two genes with seven- and six-repeat TPI domains from Nicotiana attenuata from the potato (Solanum tuberosum) PI-II family. To determine whether endogenous TPIs in N. attenuata function defensively against the native herbivores, hornworm (Manduca sexta) and mirids (Tupiocoris notatus), we expressed 175 bp of the seven-domain pi from N. attenuata in an antisense orientation in a TPI-producing genotype to reduce TPI expression and expressed the full-length seven-domain pi in a sense orientation under control of a constitutive promoter to restore TPI activity in a natural genotype from Arizona unable to produce TPIs. Constitutive and inducible TPI production in two antisense lines were diminished by 80% to 90% and 33% to 52%, respectively, and sense expression restored 67% of the activity found in the TPI-producing genotype after caterpillar attack in the TPI-deficient A genotype. Hornworm larvae fed on genotypes with low or no TPI activity grew faster, had higher survivorship, and produced heavier pupae than those that fed on genotypes with high TPI activity. T. notatus showed higher preference for genotypes with low or no TPI activity than for genotypes with high TPI levels. We conclude that endogenous TPIs are an effective defense against these native herbivores.

http://www.plantphysiol.org/content/plantphysiol/134/3/1181.full.pdf

Klaus Gase

Papers

Nicotine's defensive function in nature.

Field experiments with transformed plants reveal the sense of floral scents

Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system

Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9

Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses