Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth–promoting bacteria and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens and insect herbivores. A wide variety of root-associated mutualists, including Pseudomonas, Bacillus, Trichoderma, and mycorrhiza species sensitize the plant immune system for enhanced defense without directly activating costly defenses. This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in our understanding of ISR signaling and systemic defense priming. The central role of the root-specific transcription factor MYB72 in the onset of ISR and the role of phytohormones and defense regulatory proteins in the expression of ISR in aboveground plant parts are highlighted. Finally, the ecological function of ISR-inducing microbes in the root microbiome is discussed.

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Induced systemic resistance by beneficial microbes

Plant responses to the projected future levels of CO2 were first characterized in short-term experiments lasting days to weeks. However, longer term acclimation responses to elevated CO2 were subsequently discovered to be very important in determining plant and ecosystem function. Free-Air CO2 Enrichment (FACE) experiments are the culmination of efforts to assess the impact of elevated CO2 on plants over multiple seasons and, in the case of crops, over their entire lifetime. FACE has been used to expose vegetation to elevated concentrations of atmospheric CO2 under completely open-air conditions for nearly two decades. This review describes some of the lessons learned from the long-term investment in these experiments. First, elevated CO2 stimulates photosynthetic carbon gain and net primary production over the long term despite down-regulation of Rubisco activity. Second, elevated CO2 improves nitrogen use efficiency and, third, decreases water use at both the leaf and canopy scale. Fourth, elevated CO2 stimulates dark respiration via a transcriptional reprogramming of metabolism. Fifth, elevated CO2 does not directly stimulate C4 photosynthesis, but can indirectly stimulate carbon gain in times and places of drought. Finally, the stimulation of yield by elevated CO2 in crop species is much smaller than expected. While many of these lessons have been most clearly demonstrated in crop systems, all of the lessons have important implications for natural systems.

Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE

Systemic acquired resistance (SAR) is an induced immune mechanism in plants. Unlike vertebrate adaptive immunity, SAR is broad spectrum, with no specificity to the initial infection. An avirulent pathogen causing local programmed cell death can induce SAR through generation of mobile signals, accumulation of the defense hormone salicylic acid, and secretion of the antimicrobial PR (pathogenesis-related) proteins. Consequently, the rest of the plant is protected from secondary infection for a period of weeks to months. SAR can even be passed on to progeny through epigenetic regulation. The Arabidopsis NPR1 (nonexpresser of PR genes 1) protein is a master regulator of SAR. Recent study has shown that salicylic acid directly binds to the NPR1 adaptor proteins NPR3 and NPR4, regulates their interactions with NPR1, and controls NPR1 protein stability. However, how NPR1 interacts with TGA transcription factors to activate defense gene expression is still not well understood. In addition, redox regulators, the m...

Systemic Acquired Resistance: Turning Local Infection into Global Defense

"The Challenge The unimpeded growth of greenhouse gas emissions is raising the earth’s temperature. The consequences include melting glaciers, more precipitation, more and more extreme weather events, and shifting seasons. The accelerating pace of climate change, combined with global population and income growth, threatens food security everywhere. Agriculture is extremely vulnerable to climate change. Higher temperatures eventually reduce yields of desirable crops while encouraging weed and pest proliferation. Changes in precipitation patterns increase the likelihood of short-run crop failures and long-run production declines. Although there will be gains in some crops in some regions of the world, the overall impacts of climate change on agriculture are expected to be negative, threatening global food security. Populations in the developing world, which are already vulnerable and food insecure, are likely to be the most seriously affected. In 2005, nearly half of the economically active population in developing countries—2.5 billion people—relied on agriculture for its livelihood. Today, 75 percent of the world’s poor live in rural areas. This Food Policy Report presents research results that quantify the climate-change impacts mentioned above, assesses the consequences for food security, and estimates the investments that would offset the negative consequences for human well-being. This analysis brings together, for the first time, detailed modeling of crop growth under climate change with insights from an extremely detailed global agriculture model, using two climate scenarios to simulate future climate. The results of the analysis suggest that agriculture and human well-being will be negatively affected by climate change: * In developing countries, climate change will cause yield declines for the most important crops. South Asia will be particularly hard hit. * Climate change will have varying effects on irrigated yields across regions, but irrigated yields for all crops in South Asia will experience large declines. * Climate change will result in additional price increases for the most important agricultural crops–rice, wheat, maize, and soybeans. Higher feed prices will result in higher meat prices. As a result, climate change will reduce the growth in meat consumption slightly and cause a more substantial fall in cereals consumption. * Calorie availability in 2050 will not only be lower than in the no–climate-change scenario—it will actually decline relative to 2000 levels throughout the developing world. * By 2050, the decline in calorie availability will increase child malnutrition by 20 percent relative to a world with no climate change. Climate change will eliminate much of the improvement in child malnourishment levels that would occur with no climate change. * Thus, aggressive agricultural productivity investments of US$7.1–7.3 billion are needed to raise calorie consumption enough to offset the negative impacts of climate change on the health and well-being of children." from Text

Climate Change: Impact on Agriculture and Costs of Adaptation

Symbioses between plants and beneficial soil microorganisms like arbuscular-mycorrhizal fungi (AMF) are known to promote plant growth and help plants to cope with biotic and abiotic stresses. Profound physiological changes take place in the host plant upon root colonization by AMF affecting the interactions with a wide range of organisms below- and above-ground. Protective effects of the symbiosis against pathogens, pests, and parasitic plants have been described for many plant species, including agriculturally important crop varieties. Besides mechanisms such as improved plant nutrition and competition, experimental evidence supports a major role of plant defenses in the observed protection. During mycorrhiza establishment, modulation of plant defense responses occurs thus achieving a functional symbiosis. As a consequence of this modulation, a mild, but effective activation of the plant immune responses seems to occur, not only locally but also systemically. This activation leads to a primed state of the plant that allows a more efficient activation of defense mechanisms in response to attack by potential enemies. Here, we give an overview of the impact on interactions between mycorrhizal plants and pathogens, herbivores, and parasitic plants, and we summarize the current knowledge of the underlying mechanisms. We focus on the priming of jasmonate-regulated plant defense mechanisms that play a central role in the induction of resistance by arbuscular mycorrhizas.

Mycorrhiza-Induced Resistance and Priming of Plant Defenses

Inducible defenses, which provide enhanced resistance after initial attack, are nearly universal in plants. This defense signaling cascade is mediated by the synthesis, movement, and perception of jasmonic acid and related plant metabolites. To characterize the long-term persistence of plant immunity, we challenged Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum) with caterpillar herbivory, application of methyl jasmonate, or mechanical damage during vegetative growth and assessed plant resistance in subsequent generations. Here, we show that induced resistance was associated with transgenerational priming of jasmonic acid-dependent defense responses in both species, caused caterpillars to grow up to 50% smaller than on control plants, and persisted for two generations in Arabidopsis. Arabidopsis mutants that are deficient in jasmonate perception (coronatine insensitive1) or in the biogenesis of small interfering RNA (dicer-like2 dicer-like3 dicer-like4 and nuclear RNA polymerase d2a nuclear RNA polymerase d2b) do not exhibit inherited resistance. The observation of inherited resistance in both the Brassicaceae and Solanaceae suggests that this trait may be more widely distributed in plants. Epigenetic resistance to herbivory thus represents a phenotypically plastic mechanism for enhanced defense across generations.

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Herbivory in the Previous Generation Primes Plants for Enhanced Insect Resistance

Elevated levels of atmospheric carbon dioxide (CO2), a consequence of anthropogenic global change, can profoundly affect the interactions between crop plants and insect pests and may promote yet another form of global change: the rapid establishment of invasive species. Elevated CO2 increased the susceptibility of soybean plants grown under field conditions to the invasive Japanese beetle (Popillia japonica) and to a variant of western corn rootworm (Diabrotica virgifera virgifera) resistant to crop rotation by down-regulating gene expression related to defense signaling [lipoxygenase 7 (lox7), lipoxygenase 8 (lox8), and 1-aminocyclopropane-1-carboxylate synthase (acc-s)]. The down-regulation of these genes, in turn, reduced the production of cysteine proteinase inhibitors (CystPIs), which are specific deterrents to coleopteran herbivores. Beetle herbivory increased CystPI activity to a greater degree in plants grown under ambient than under elevated CO2. Gut cysteine proteinase activity was higher in beetles consuming foliage of soybeans grown under elevated CO2 than in beetles consuming soybeans grown in ambient CO2, consistent with enhanced growth and development of these beetles on plants grown in elevated CO2. These findings suggest that predicted increases in soybean productivity under projected elevated CO2 levels may be reduced by increased susceptibility to invasive crop pests.

Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects.

Hemipteran insects are devastating pests of crops due to their wide host range, rapid reproduction, and ability to transmit numerous plant-infecting pathogens as vectors. While the field of plant-virus-vector interactions has flourished in recent years, plant-bacteria-vector interactions remain poorly understood. Leafhoppers and psyllids are by far the most important vectors of bacterial pathogens, yet there are still significant gaps in our understanding of their feeding behavior, salivary secretions, and plant responses as compared to important viral vectors, such as whiteflies and aphids. Even with an incomplete understanding of plant-bacteria-vector interactions, some common themes have emerged: 1) all known vector-borne bacteria share the ability to propagate in the plant and insect host; 2) particular hemipteran families appear to be incapable of transmitting vector-borne bacteria; 3) all known vector-borne bacteria have highly reduced genomes and coding capacity, resulting in host-dependence; and 4) vector-borne bacteria encode proteins that are essential for colonization of specific hosts, though only a few types of proteins have been investigated. Here, we review the current knowledge on important vector-borne bacterial pathogens, including Xylella fastidiosa, Spiroplasma spp., Liberibacter spp., and 'Candidatus Phytoplasma spp.’. We then highlight recent approaches used in the study of vector-borne bacteria. Finally, we discuss the application of this knowledge for control and future directions that will need to be addressed in the field of vector-plant-bacteria interactions.

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Vector-Borne Bacterial Plant Pathogens: Interactions with Hemipteran Insects and Plants.

The Mi-1.2 gene, identified from wild varieties of tomato, Solanum peruvianum (Mill) (Solanaceae), has been incorporated into near-isogenic commercial varieties of tomato and has been shown to confer resistance to three different species of phloem feeders: aphids, whiteflies, and nematodes. The results presented here show that plants bearing Mi-1.2 were also resistant to the tomato psyllid, Bactericerca [Paratrioza] cockerelli (Sulc) (Homoptera: Psyllidae), a serious pest of tomato, Solanum lycopersicon (Mill), in the western half of North America. In choice studies, tomato psyllids preferred to settle on plants that did not contain the gene [Moneymaker (mi-1.2)] compared to near-isogenic plants with the gene [Motelle (Mi-1.2)]. As a result, total oviposition was higher on the susceptible variety, although no-choice studies indicated that there were no differences in numbers of eggs laid by individual females on either variety. Survival from egg to adult was higher on plants lacking the gene compared to plants containing the gene. However, there were no differences in total development time of individuals reared from either variety. The results suggest that mechanisms of resistance to the tomato psyllid observed in plants bearing the Mi-1.2 gene are distinct from the mechanisms of resistance to the three phloem feeders examined in other studies.

Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi‐1.2 gene

Many plant viruses depend on aphids and other phloem-feeding insects for transmission within and among host plants. Thus, viruses may promote their own transmission by manipulating plant physiology to attract aphids and increase aphid reproduction. Consistent with this hypothesis, Myzus persicae (green peach aphids) prefer to settle on Nicotiana benthamiana infected with Turnip mosaic virus (TuMV) and fecundity on virus-infected N. benthamiana and Arabidopsis thaliana (Arabidopsis) is higher than on uninfected controls. TuMV infection suppresses callose deposition, an important plant defense, and increases the amount of free amino acids, the major source of nitrogen for aphids. To investigate the underlying molecular mechanisms of this phenomenon, 10 TuMV genes were over-expressed in plants to determine their effects on aphid reproduction. Production of a single TuMV protein, nuclear inclusion a-protease domain (NIa-Pro), increased M. persicae reproduction on both N. benthamiana and Arabidopsis. Similar to the effects that are observed during TuMV infection, NIa-Pro expression alone increased aphid arrestment, suppressed callose deposition and increased the abundance of free amino acids. Together, these results suggest a function for the TuMV NIa-Pro protein in manipulating the physiology of host plants. By attracting aphid vectors and promoting their reproduction, TuMV may influence plant-aphid interactions to promote its own transmission.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.12417

Clare L. Casteel

Papers

Herbivory in the Previous Generation Primes Plants for Enhanced Insect Resistance

Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects.

Vector-Borne Bacterial Plant Pathogens: Interactions with Hemipteran Insects and Plants.

Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi‐1.2 gene

The NIa-Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid).