Martin Heil

Center for Research and Advanced Studies of the National Polytechnic Institute | Cinvestav · Departamento de Ingeniería Genética (Irapuato)

Mammals sense self or non-self extracellular or extranuclear DNA fragments (hereinafter collectively termed eDNA) as indicators of injury or infection and respond with immunity. We hypothesised that eDNA acts as a damage-associated molecular pattern (DAMP) also in plants and that it contributes to self versus non-self discrimination. Treating plant...

Background The plant immune response to DNA is highly self/nonself-specific. Self-DNA triggered stronger responses by early immune signals such as H2O2 formation than nonself-DNA from closely related plant species. Plants lack known DNA receptors. Therefore, we aimed to investigate whether a differential sensing of self-versus nonself DNA fragments...

The coronavirus disease 2019 (COVID-19) pandemic triggered an unprecedented concentration of economic and research efforts to generate knowledge at unequalled speed on deregulated interferon type I signalling and nuclear factor kappa light chain enhancer in B-cells (NF-κB)-driven interleukin (IL)-1β, IL-6, IL-18 secretion causing cytokine storms. T...

Introduction Stress-induced volatile organic compounds (VOCs) that induce plant immunity bear potential for biocontrol. Here, we explore the potential of nonanal to enhance the seed yield of common bean (Phaseolus vulgaris) under open field conditions that are realistic for smallholder farmers. Methods and results Using plastic cups with a nonanal...

Abstract The accumulation of DNA in the cytoplasm or extracellular space is a signal of danger. Plants respond to this signal with a self/non-self-specific activation of early immune signalling events. Here, we asked whether this specificity translates to fitness-relevant resistance to natural enemies. We treated common bean (Phaseolus vulgaris) pl...

Photosynthesis is a vital process for the planet. Its estimation involves the measurement of different variables and its processing through a mathematical model. This article presents a black-box mathematical model to estimate the net photosynthesis and its digital implementation. The model uses variables such as: leaf temperature, relative leaf hu...

Plant roots recruit most prokaryotic members of their root microbiota from the locally avail- able inoculum, but knowledge on the contribution of native microorganisms to the root microbiota of crops in native versus non-native areas remains scarce. We grew common bean (Phaseolus vulgaris) at a field site in its centre of domestication to character...

All organisms on the planet use Damage Associated Molecular Patterns (DAMPs) to signal that injury has occurred, in order to initiate repair, remodeling, and immunity. It suggests that DAMPs and DAMPs-initiated signaling systems might be the most primordial form of innate immunity and tissue repair systems in living organisms before sophisticated i...

Root colonizing Trichoderma fungi can stimulate plant immunity, but net effects are strain × cultivar-specific and changing ambient conditions further contribute to variable outcomes. Here, we used four Trichoderma spp. to inoculate seeds of four common bean (Phaseolus vulgaris) cultivars and explored in three different experimental setups the effe...

The inhibitory effect of extracellular DNA (exDNA) on the growth of conspecific individuals was demonstrated in different kingdoms. In plants, the inhibition has been observed on root growth and seed germination, demonstrating its role in plant–soil negative feedback. Several hypotheses have been proposed to explain the early response to exDNA and...

Danger signals trigger immune responses upon perception by a complex surveillance system. Such signals can originate from the infectious nonself or the damaged self, the latter termed damage-associated molecular patterns (DAMPs). Here, we apply Matzinger’s danger model to plant innate immunity to discuss the adaptive advantages of DAMPs and their i...

Numerous plant-derived volatile organic compounds (VOCs) induce the expression of resistance-related genes and thereby cause an “associational resistance” in neighbouring plants. However, VOCs can also be sequestered by plant cuticular waxes. In case that they maintain their biological activity, such sequestered VOCs could generate a “passive” asso...

The poster aims to highlight the complex volatile-mediated crosstalk among different genotypes of Phaseolus vulgaris and three Trichoderma species, through the high resolution proton transfer reaction mass spectrometry (PTR-QiTOF).

Inflammation, over-reacting innate immunity, and CD4+ T cell depletion are hallmarks of HIV-1 infection. Self-DNA is usually not considered in the context of HIV-1-associated inflammation, although self-DNA contributes to inflammation in diverse pathologies, including autoimmune diseases, cancer, multiorgan failure after trauma, and even virus infe...

Plants, fungi and mammals share multiple elements of their innate immune system, including the perception of ‘damage-associated molecular patterns’ (DAMPs) (Heil and Land 2014). The most recent milestone in this development comes from Grandellis et al. (2019). In the February issue of Planta, they describe an innate immune response in Arabidopsis...

The accumulation of nucleic acids in aberrant compartments is a signal of danger: fragments of cytosolic or extracellular self-DNA indicate cellular dysfunctions or disruption, whereas cytosolic fragments of nonself-DNA or RNA indicate infections. Therefore, nucleic acids trigger immunity in mammals and plants. In mammals, endosomal Toll-like recep...

Poster for the PhD-course "Plant communication and trophic interactions" (Flen, Sweden). Soilborne Trichoderma spp. fungi are used as biocontrol agents that promote plant growth and disease resistance. Both host-plant and fungus contribute to these effects, making the net outcome highly context-dependent, and little is known on the effects on the c...

Plants in more than 100 families secrete extrafloral nectar (EFN) to establish food-for-protection mutualisms with ants. Facultative ant-plants secrete EFN as a jasmonic acid (JA)-dependent response to attract generalist ants. In contrast, obligate ant-plants like the Central American “Swollen-Thorn Acacias” are colonized by specialized ants, altho...

Psittacanthus calyculatus is a hemiparasitic plant that infects a wide range of trees. Mainly the biology reproduction of this mistletoe lies in bright colored flower development. Furthermore, it uses the nectar secretion as the only reward to engage different flower visitors. We investigated the physiological mechanisms of the flower phenology per...

Domestication reduced the resistance of most crops which, therefore, require an ever-increasing application of pesticides. Nevertheless, in most domesticated species, the resistance against herbivores and disease agents can be activated by so-called elicitors. Here, we review various strategies of biological pest control and particularly focus on d...

Fungi emit a diverse blend of volatile organic compounds (VOCs) that mediate multiple fungus-fungus interactions. Plants emit VOCs as well, which can serve as resistance-inducing signals but might also act as direct resistance agents. We screened 22 VOCs that are emitted from infected plants for putative inhibitory effects on three fungal phytopath...

p> Background: Little is known on factors determining infection of tropical plants by fungal pathogens, although multiple studies on model species show that light conditions affect the two major hormones that control resistance in plants to enemies. This is the first study using a natural population of a wild tropical plant to relate light conditio...

Resumen El frijol común es la leguminosa de mayor consumo en México. Su rendimiento se ve disminuido por la "antracnosis", causada por el hongo Colletotrichum lindemuthianum, ocasionando pérdidas de hasta 100%. Sin embargo, cuando una planta es infectada, emite compuestos orgánicos volátiles (COVs), compuestos utilizados por las plantas como mecani...

Ants are probably the most dominant insect family on earth, and flowering plants have been the dominant plant group on land for more than 100 million years. In recent decades, human activities have degraded natural environments with unparalleled speed and scale, making it increasingly apparent that interspecific interactions vary not only under dif...

Host manipulation refers to the expression of a host phenotype that is partly under the genetic control of a parasite. This phenomenon can enhance parasite transmission rates and is responsible for biological marvels such as “Zombie‐ants” and the “fatal attraction” of Toxoplasma ‐infected rodents to their feline predators. Such host manipulation ha...

Establishing a horizontally transmitted mutualism is a critical step for many organisms, particularly when an individual can engage with only one partner over its lifetime. Ant foundresses shed their wings before they start to lay eggs, which makes host choice particularly critical for plant‐ants that exclusively colonize myrmecophytes. Volatile or...

Phaseolus lunatus (lima bean) has been a model organism to understand direct and indirect defenses against herbivores. We investigated the identity and diversity of endophytic fungi associated with young, mature and old leaves of lima bean in its natural environment. We recovered 758 isolates that were identified and classified in 142 fungal specie...

Naturally plants respond to pests and infections with the emission of volatile organic compounds (VOCs).Which are involved indirect in attract pollinators or predators of herbivores, also they play roles direct way as insect deterrents and have antimicrobial properties.In this project, we focus on the role played by VOCsin the resistance of plants...

Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta‐analysis to characterize patterns of covariation in CCDs and ide...

El frijol común es la leguminosa de mayor consumo en México. Su rendimiento se ve disminuido por la "antracnosis", causada por el hongo Colletotrichum lindemuthianum, ocasionando pérdidas de hasta 100%. Sin embargo, cuando una planta es infectada, emite compuestos orgánicos volátiles (COVs), compuestos utilizados por las plantas como mecanismo de d...

Endophyte fungi live within all plants investigated so far. These fungi do not cause disease symptoms and can also show beneficial effects to its host. Although it has been found a great diversity inside one tissue, it is still unknown how it is maintained the interactions inside the plant. Volatile organic compounds could be an excellent sign to m...

All multi-cellular organisms share the necessity to perceive damage and to employ an adequate immune response to withstand injury and infection. The role of damage-associated molecular patterns (DAMPs) in the mammalian adaptive immune system and in allograft rejection was discovered by Polly Matzinger and Walter Land (Land et al., 1994;Matzinger, 1...

The 'adaptive host manipulation' hypothesis predicts that parasites can enhance their transmission rates via manipulation of their host's phenotype. For example, many plant pathogens alter the nutritional quality of their host for herbivores that serve as their vectors. However, herbivores, including non-vectors, might cause additional alterations...

Defense priming conditions diverse plant species for the superinduction of defense, often resulting in enhanced pest and disease resistance and abiotic stress tolerance. Here, we propose a guideline that might assist the plant research community in a consistent assessment of defense priming in plants.

Parasites must overcome host immunity and change hosts for dispersal. Therefore, seemingly odd behaviors of parasitized animals, like those exhibited by “Zombie ants” or the “fatal attraction” of mammals to their predators, have been explained as the extended phenotype of parasites that manipulate their hosts for transmission enhancement. Manipulat...

Wounded nightshade leaves secrete a sugary liquid that, like extrafloral nectar (EFN), attracts ants as defence against herbivores. The secretion of these droplets requires no detectable nectary tissue, showing how little it takes to produce a functioning nectary. Easy de novo formation of extrafloral nectaries explains their 'scattered' phylogenet...

Thousands of plant species throughout tropical and temperate zones secrete extrafloral nectar to attract ants, whose presence provides an indirect defense against herbivores. Extrafloral nectaries are located close to flowers and may modify competition between ants and pollinators. Here, we used Lima bean (Phaseolus lunatus L.) to study the plants...

Volatile compounds and extrafloral nectar are common defenses of wild plants; however, in crops they bear an as-yet underused potential for biological control of pests and diseases. Odor emission and nectar secretion are multigene traits in wild plants, and thus form difficult targets for breeding. Furthermore, domestication has changed the capacit...

Plants that express resistance to herbivores emit volatile organic compounds ( VOC s) that can trigger resistance responses in undamaged neighbours. Recent reports indicate that VOC s can also trigger the resistance to pathogens, an effect that might be due to different mechanisms: the priming of an induced expression of resistance genes in the rec...

Ant–plant interactions are classic examples of defensive mutualisms and have served as model systems to study the ecology and evolution of mutualisms since the 19th century. Ant–plant mutualisms range in specificity from myrmecophilic (ant-loving) plants, which attract free-living ants to obtain defense against herbivores, to obligate myrmecophytes...

A recent study reports partner manipulation for an interaction that was considered a reward-for-defence mutualism. Secretions of lycaenid caterpillars altered ant locomotion and aggressiveness, likely by manipulating dopaminergic signalling. This study opens the question whether such manipulation is common and whether manipulation necessarily chara...

Abstract Four varieties of common bean (Phaseolus vulgaris) classified according to their level of resistance to Colletotrichum lindemuthianum (causal agent of anthracnose) were used, identifying a resistant and susceptible cultivar line. Subsequently, they were analyzed and identified volatile organic compounds (VOC’s) emitted by the plants resist...

The mutualistic relationships between certain ant and aphid species are well known, the primary benefits being protection for the aphids and carbohydrate-rich honeydew for the ants. Questions remain, however, as to the exact semiochemical factors that establish and maintain such relationships. In this study, we used a series of treatments and assoc...

Nitrogen plays a central role in most metabolic processes and therefore represents a critical element in the growth of all organisms (Mattson, 1980). However, whereas many prokaryotes can assimilate atmospheric N2 and then are autotrophs for this nutrient, the higher organisms such as plants, animals, and fungi do not harbor this important physiolo...

Plants secrete extrafloral nectar (EFN) as an induced defense against herbivores. EFN contains not only carbohydrates and amino acids but also pathogenesis-related proteins and other protective enzymes, making EFN an exclusive reward. EFN secretion is commonly induced after wounding, likely owing to a jasmonic acid-induced cell wall invertase, and...

Plants establish multiple interactions with microorganisms. The most well-known examples comprise mutualistic interactions of plant roots with fungi [mycorrhiza] and bacteria [rhizobia] and parasitic interactions with plant pathogens aboveground and belowground. However, we are just starting to discover that all parts of a plant in nature are invar...

The response to mechanical damage is crucial for the survival of multicellular organisms, enabling their adaptation to hostile environments. Trichoderma atroviride, a filamentous fungus of great importance in the biological control of plant diseases, responds to mechanical damage by activating regenerative processes and asexual reproduction (conidi...

Mutualisms require protection from non-reciprocating exploiters. Pseudomyrmex workers that engage in an obligate defensive mutualism with Acacia hosts feed exclusively on the sucrose-free extrafloral nectar (EFN) that is secreted by their hosts, a behaviour linking ant energy supply directly to host performance and thus favouring reciprocating beha...

Plants require reliable mechanisms to detect injury. Danger signals or “damage-associated molecular patterns” (DAMPs) are released from stressed host cells and allow injury detection independently of enemy-derived molecules. We studied the response of common bean (Phaseolus vulgaris) to the application of leaf homogenate as a source of DAMPs and me...

Multicellular organisms suffer injury and serve as hosts for microorganisms. Therefore, they require mechanisms to detect injury and to distinguish the self from the non-self and the harmless non-self (microbial mutualists and commensals) from the detrimental non-self (pathogens). Danger signals are “damage-associated molecular patterns” (DAMPs) th...

Plants respond to mechanical wounding, herbivore feeding or infection by pathogens with the release of volatiles. Small C6 molecules termed green-leaf volatiles form a general element in most of these blends; however, the overall composition is usually sufficiently specific that other organisms are able to determine the nature of the attacker. Rece...

Symptomless 'type II' fungal endophytes colonize their plant host horizontally and exert diverse effects on its resistance phenotype. Here, we used wild Lima bean (Phaseolus lunatus) plants that were experimentally colonized with one of three strains of natural endophytes (Bartalinia pondoensis, Fusarium sp., or Cochliobolus lunatus) to investigate...

Plants secrete extrafloral nectar (EFN) that attracts predators. The efficiency of the resulting anti-herbivore defense depends on the quantity and spatial distribution of EFN. Thus, according to the optimal defense hypothesis (ODH), plants should secrete EFN on the most valuable organs and when herbivore pressure is high. Ricinus communis plants s...

The role of plant polyphenols as defenses against insect herbivores is controversial. We combined correlative field studies across three geographic regions (Northern Mexico, Southern Mexico, and Costa Rica) with induction experiments under controlled conditions to search for candidate compounds that might play a defensive role in the foliage of the...

Endophytic fungi colonize plants without causing symptoms of disease and can enhance the resistance of their host to pathogens. We cultivated 53 fungal strains from wild lima bean (Phaseolus lunatus) and investigated their effects on pathogens using in vitro assays and experiments in planta. Most strains were annotated as Rhizopus, Fusarium, Penici...

The major shortcomings of chemically induced resistance in crops to disease are that resistance enhancement comes at a cost to the plant that might cause significant reductions in yield in spite of a successful resistance induction. Also, the efficiency of the resistance induction is highly context dependent and depends, in part, on the genetic ide...

In nature, plants are exposed to a number of herbivores that my attack them at the same or different times during the season. Studies have shown that a first attack can induce chemical changes in a plant that affect the performance of subsequent herbivores. This is usually studied for insects that feed on the same plant tissue. Using wild lima bean...

Plant pathogens affect the fitness of their hosts and maintain biodiversity. However, we lack theories to predict the type and intensity of infections in wild plants. Here we demonstrate using fungal pathogens of tropical plants that an examination of the life histories of hosts and pathogens can reveal general patterns in their interactions. Funga...

In spite of the ecological and evolutionary importance of nectar, mechanisms controlling its synthesis and secretion remain largely unknown. It is widely believed that nectar is 'secreted phloem sap', but current research reveals a biochemical complexity that is unlikely to stem directly from the phloem. We used the short daily peak in the producti...

Nectar secretion serves two important mutualisms. Floral nectar (FN) mediates pollination whereas extrafloral nectar (EFN) serves the indirect defence against herbivores. Research over the last decade has focused on the anti-microbial protection of nectars. The Nectar Redox Cycle consists of several nectar proteins (nectarins) in FN of ornamental t...

Mutualisms are commonly threatened by parasites and cheaters: species that exploit the host-derived resources without providing an adequate service. Here, we summarize mechanisms for the stabilization of obligate defensive ant–plant mutualisms, a typical element of tropical lowland forests. Host plants exert partner choice and can sanction non-defe...

Myrmecophytic Acacia species produce food bodies (FBs) to nourish ants of the Pseudomyrmex ferrugineus group, with which they live in an obligate mutualism. We investigated how the FBs are protected from exploiting nonmutualists. Two-dimensional gel electrophoresis of the FB proteomes and consecutive protein sequencing indicated the presence of sev...

Endophytes infect living plant tissues without causing symptoms of disease. Indeed, many of them contribute to the resistance phenotype of their host. However, fungal endophytes are generally closely related to plant pathogens, fungi that either develop within living host tissue (biotrophic fungi) or that kill the host cells and then live in the de...

Plants respond to herbivore damage with the release of volatile organic compounds (VOCs). This indirect defense can cause ecological costs when herbivores themselves use VOCs as cues to localize suitable host plants. Can VOCs reliably indicate food plant quality to herbivores? WE DETERMINED THE CHOICE BEHAVIOR OF HERBIVOROUS BEETLES (CHRYSOMELIDAE:...

Plants secrete nectar to attract pollinators and indirect defenders. The chemical contents of both floral and extrafloral nectar appear adapted to attract and nourish these two classes of animal mutualists. Being rich in sugars and amino acids, however, nectar also requires protection from nectar robbers and infecting micro-organisms. This role is...

Extrafloral nectar (EFN) plays an important role as plant indirect defence through the attraction of defending ants. Like all rewards produced in the context of a mutualism, however, EFN is in danger of being exploited by non-ant consumers that do not defend the plant against herbivores. Here we asked whether plants, by investing more in EFN, can i...