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Primary or Obligatory Symbiont Buchnera aphidicola

Plant phloem is an unbalanced source of nutrients, very rich in sugar but with low amounts of vitamins and essential amino acids such as methionine and tryptophan (Sandström and Moran, 1999; Douglas et al., 2006b). For example, essential amino acids represent only 8.2% of the total amino acids in the phloem of the fava beans (Douglas et al., 2006b). Compensation for this unbalanced diet is ensured by the obligatory symbiosis established with the bacteria Buchnera aphidicola (Baumann et al., 1997; Sapp, 2002). This is one of the oldest symbiosis, established 160-180 million years ago, which is likely at the origin of the diversification of aphid phloemophagous insects. B. aphidicola is a γ-proteobacterium confined to specialized aphid cells, known as primary bacteriocytes (Figure 12). These symbionts are vertically transmitted from the mother to the offspring and account for a large part of the aphid microbiome. Numerous studies have shown that aphids can synthesize the nine essential amino acids in association with this endosymbiotic bacteria (Douglas et al., 2006b; Douglas, 2014; Boulain et al., 2018). In the course of evolution, the genome of Buchnera has been drastically reduced (about 500 kb), notably due to the loss of genes involved in its pathogenicity, redundant genes and regulatory genes (Gil et al., 2002; Van Ham et al., 2003). In contrast, genes involved in the biosynthesis of essential amino acids have been conserved, unlike those that were part of non-essential amino acid synthesis pathways.
Figure 12 The bacteriome and bacteriocytes. Bacteriocytes localize to the aphid abdomen and surround the gut. The ensemble of bacteriocytes constitutes the aphid bacteriome (left). Staining of B. aphidicola (green) reveals each bacteriocyte of the bacteriome (centre). Right, Magnification of one bacteriocyte filled with green B. aphidicola cells (yellow arrow pointing the nucleus).

Facultative Symbionts

In addition to a primary symbiont, A. pisum individuals can host one or two (rarely more) other facultative symbionts, also called secondary symbionts. To date, nine have been described in aphids, including Serratia symbiotica, Regiella insecticola, Hamiltonella defensa, Spiroplasma sp., Rickettsia sp., Fukatsuia symbiotica (previously PAXS), Rickettsiella sp and Wolbachia (Oliver et al., 2010; Guo et al., 2017; Guyomar et al., 2018). These secondary symbionts can be found alone in most of the cases or with another symbiont in aphid individuals. Some associations are often observed between Serratia and Rickettsiella. Single symbiont infection has been proven to be more stable than multiple infection (Frantz et al., 2009; Guay et al., 2010; Tsuchida et al., 2011). Some of these facultative symbionts can be located in specialized cells bordering the bacteriocytes (sheath cells), in secondary bacteriocytes, in the aphid hemocytes or freely circulating in the hemolymph (Figure 13) (Moran et al., 2005; Oliver et al., 2010; Schmitz et al., 2012). These symbionts are also maternally inherited but may also be transmitted sporadically horizontally (Oliver et al., 2010). Most of these facultative symbionts are pleomorphic (i.e. change in their morphology depending on the conditions) under different symbiotic conditions.
Figure 13 Localization of A. pisum secondary symbionts in its host tissues. In situ hybridization of B. aphidicola (green, A-C) and S. symbiotica (A), H. defensa (B) and R. insecticola (C) (red) in aphid embryos. The nucleus is stained in blue. Arrows indicate secondary symbionts in bacteriocytes; arrowheads indicate secondary symbionts in sheath cells, which localize to the bacteriome periphery and associate with the primary bacteriocytes. Scale bar, 100 μm (adapted from Moran et al., 2005).
The presence of specific symbiont mainly depends on the aphid biotype (for pea aphid, the legume plant on which the biotype is specialized), the host plant and the presence of natural enemies. For instance, S. symbiotica and Rickettsia sp. are common in aphids’ biotypes infecting peas or beans; R. insecticola is specially found in the clover biotype; H. defensa in the alfalfa and Spiroplasma sp. in the clover and alfalfa biotypes (Frantz et al., 2009).
Thanks to their extended phenotypes, facultative symbionts can greatly influence the ecology and the physiology of their hosts, and in several ways (Oliver et al., 2010). They can notably help aphids to deal with various different stresses (Table 1) (Oliver et al., 2010). When temperature increases, aphid performance (survival, development time and fecundity) is improved in the presence of S. symbiotica. (Russell and Moran, 2006). H. defensa protects aphids against parasitoid wasps thanks to the presence of a bacteriophage (APSE), some strains producing toxins that kill the wasp embryo (Oliver et al., 2003; Oliver and Higashi, 2019).
The facultative symbiont R. insecticola induces aphid resistance to entomopathogenic fungus (Ferrari, 2004; Scarborough et al., 2005; Łukasik et al., 2013a, 2013b). Facultative symbionts can also influence the interaction between aphid and their predators. The symbiont Rickettsiella can change aphid colour from pink to green, which protects aphids from predators on its host plants (Tsuchida et al., 2011). Finally, several studies pointed the role of facultative symbionts in the adaptation to the plant. A better performance on the pea and clover plants was associated with the presence of R. insecticola (Tsuchida et al., 2004) but this phenotype seems to depend on the complex association with host aphid and plant genotypes (Ferrari et al., 2007; Wulff and White, 2015). The Arsenophonus symbiont presence improved the performance of the soybean aphid (Aphis glycines) on its host plant (Wulff et al., 2013; Wulff and White, 2015) and that of the spotted alfalfa aphids on their black locust trees hosts (Wagner et al., 2015).
Overall, these symbionts can help aphids improve their food performance, protect them against fungi and parasitoids, give them tolerance to high temperatures, and cause variations in their colour. Some of them also have an impact on the immune components (Schmitz et al., 2012; Laughton et al., 2016). Facultative symbionts thus influence the fitness of their host either positively or negatively. A better understanding of these traits could help us develop symbiont-based strategies to manage pests and diseases.

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Pea Aphid: Host Plant Specialization

Pea aphids have a wide range of host plants within the Fabaceae family, with about 50 host plants referenced (Hopkins et al., 2017), and several hundreds of species as potential hosts. A. pisum populations are very dense on clover (Trifolium pratense purple clover and T. repens white clover), cultivated alfalfa (Medicago sativa), peas (Pisum sativum) and beans (Vicia faba). Within the same insect species, notably variations in plant use have been frequently documented. Ecologically and genetically distinct populations are referred to as “biotype”, “host race” or “ecotype” (Diehl and Bush, 1984). A. pisum is often considered as a single insect species but it rather consists of at least 15 biotypes with distinct genetic structuration associated to their preferred host plant (not the geographic location) and differential fitness on specific host plants (Peccoud et al., 2009, 2015). These aphid biotypes are specialized to one or a few host plants and form a sympatric population due to partial reproductive segregation. The current view is that the pea aphid has undergone rapid diversification about 10 000 years ago at the time of the development of agriculture, which led to the formation of the different biotypes through host plant specialization. Interestingly, all pea aphid biotypes characterized to date perform extremely well on the universal host Vicia faba.
It is interesting to note that the infection and distribution of facultative symbionts vary considerably with biotypes (Peccoud et al., 2015). For example, H. defensa is particularly associated with pea aphids feeding on Ononis, Genista, Lotus or Medicago in France. In turn, R. insecticola and S. symbiotica were more commonly associated with pea aphids collected on Trifolium and Cytisus, respectively. A field study on alfalfa (Medicago sativa), red clover (Trifolium pratense) and hairy vetch (Vicia villosa) in North America reported that most aphids (mean = 74.2%) were infected with at least one facultative symbiont. H. defensa was found more often associated with aphids on alfalfa, Regiella with those on clover, while Serratia and Regiella were found at the same frequency on aphids on hairy vetch (Russell et al., 2013). Field studies also indicate the presence of multiple aphid-associated symbiont strains on a plant species, varying infection levels for seven species of common symbionts, and the frequent occurrence of coinfection by several species of symbionts. There are also geographical differences in the distribution of symbionts. However, how secondary symbionts influence the use of the host plant in pea aphid remains unclear. Phylogenetic analysis suggests that acquisition of symbionts often accompanies aphid host change. It is not known whether this is related to host use or other ecological factors correlated with the transition to a new host. Indeed, Tsuchida et al., 2004 found that the removal of Regiella reduced the capacity of a pea aphid clone to feed on clover, while introduction of this same Regiella in a naive aphid host (Megoura crassicauda) improved its performance on the same plant (Tsuchida et al., 2004).

Specific Plant Defence Reaction Against Aphids

Several recent studies have examined the impact of aphid feeding on plant transcription profiles and identified the putative defensive responses that occur in susceptible and resistant hosts. They demonstrated a strong induction of SA, ET, and abscisic acid (ABA) pathways after aphid infestation (Moran and Thompson, 2001; De Vos et al., 2005; Guerrieri and Digilio, 2008; Kerchev et al., 2012; Jaouannet et al., 2014; Nalam et al., 2019), whereas JA signalling seemed to be repressed (De Vos et al., 2007; Kerchev et al., 2013) hypothesized that the aphids could manipulate the SA-pathways to suppress the JA-pathway, which could be more damaging to this insect. Although manipulation of the crosstalk JA-SA was observed in several insects (Diezel et al., 2009; Chung et al., 2013b), experimental evidence supporting this hypothesis still remains unclear for plant-aphid interaction (Kerchev et al., 2013). Moreover, despite changes in the expression of marker genes, suggesting an activation of different signalling pathways, there is no increase in phytohormones levels JA, SA, and ET when A. thaliana is exposed to M. persicae (De Vos et al., 2005). Non-adapted A. pisum clones to alfalfa induce significantly higher levels of SA and JA compared to adapted ones (Sanchez-Arcos et al., 2016).
Aphids cause very little physical damage to the host plant, compared to chewing insects, thus making difficult to understand the involvement of the defence associated with JA against aphids. It is also worth noting that the role of SA and JA in plant–aphid interactions may vary among plant species. In Arabidopsis, aphid bioassays on mutant lines with altered JA or SA signalling suggest that JA limits the growth of aphid populations, whereas SA induction has neutral or even positive effects on the aphid performance.

Table of contents :

1.1 Interactions and Evolutionary Processes, the Holobiont Theory
1.2 Microbes, the New Players in the Plant-Insect Interactions
1.3 Plant Symbiosis
1.3.1 Plant Bacteria Symbiosis: The Leguminous Plants
1.3.2 The Nitrogen Fixing Symbiosis
1.3.3 The Nodules Structure
1.3.4 Nodule Nitrogen Fixation Process
1.3.5 Nodule Growth and Activity are Regulated by A Feedback Mechanism
1.3.6 Nodule Senescence
1.4 Plant Disease and Immune Response
1.5 Plants Defence Responses
1.5.1 Molecular Mechanisms in Plant Pathogen Interactions
1.5.2 Systemic Acquired Resistance and Induced Systemic Resistance
1.5.3 Hormones Involved in Plant Defence
1.6 Insects Symbiosis
1.6.1 The Aphids
1.6.2 Pea Aphid Model, Acyrthosiphon pisum
1.6.3 Primary or Obligatory Symbiont Buchnera aphidicola
1.6.4 Facultative Symbionts
1.6.5 Pea Aphid: Host Plant Specialization
1.6.6 Specific Plant Defence Reaction Against Aphids
Preliminary Experiments
Set up of the experiences with Medicago
Introduction of the 1st publication
Publication 1: Nitrogen-fixation symbiosis affects legume-aphid interactions and plant defence.
Introduction for 2nd Publication
Publication 2: Plant-aphid genotypic diversity and rhizobacteria community influence each other in three-way interactions
6.1 Effect of Plant on Aphid’s fitness
6.2 Effect of Aphid on Plant
6.3 How to explain this aphid effect?


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