Implications of the foliar phytochemical diversity of the avocado crop Persea americana cv. Hass in its susceptibility to pests and pathogens

Abstract

Phytochemical diversity (PD) can be considered as a defensive trait; it can operate through single plant secondary metabolites or usually as complex mixtures of them. We tested the more diversity-better defense hypothesis correlating the leaf plant secondary metabolites (PSMs) with the incidence of plant enemies on Hass avocado trees. We expected a negative correlation between the occurrence of plant enemies and PD metrics. Also, as intraspecific PSMs polymorphisms in plant populations are common, we studied the incidence of plant enemies on Hass avocado trees representing chemical variants (chemotypes). We expected a differential incidence of plant enemies among trees grouped by their mono and sesquiterpene + phenylpropanoid chemotypes. We analyzed foliar hexane extracts from 236 trees in 17 orchards by gas chromatography and for the incidence of red mite, thrips, whitefly, avocado branch borer, fruit rot, scab, and peduncle collar blight. The predicted negative correlation between the plant enemies’ incidence and the phytochemical metrics did not occur. To determine the relationship between enemy incidence and chemotypes we grouped the trees by cluster analysis using a matrix of PSMs in each tree. Most trees were grouped under four out of 23 chemotypes. Branch borers attacked trees of low-frequency chemotypes more frequently than trees with common chemotypes. The incidence of five plant enemies was different among the predominant chemotypes. The hypothesis of more diversity-better defense was not supported by the correlations between the phytochemical diversity and the incidence of pests and pathogens in Hass avocado orchards. Based on our results, we hypothesize that phytochemical diversity function as a defensive trait relies more on differentiation among individuals in a population than on the sole increase of chemical diversity. Also, the differential incidence of pests and pathogens on trees classified by their foliar chemotypes implies that these susceptibility or resistance markers represent potential useful tools for Hass avocado orchard pest management.

Understanding the phytochemical diversity of plants: Quantification, variation and ecological function

“…It can also affect the diversity or structure of the community of herbivores feeding on host plants (Richards et al 2015, Volf et al 2018, Harrison et al 2018, Cosmo et al 2021, affect tri-trophic interactions (Wan et al 2017, Slinn et al 2018, and shape the diversity of the surrounding plant and microbe communities (Iason et al 2005, Zhang et al 2023. Other studies have instead found that intermediate or high levels of phytochemical diversity might be disadvantageous (Sternberg et al 2012, Pais et al 2018, found no/limited effects of it on herbivory (Torres-Gurrola et al 2011, Schuldt et al 2012, Espinosa-García et al 2021, or found no differences between different populations (Wolf et al 2012). On balance, results from these studies suggest that an increased phytochemical diversity is often, but not always, beneficial for plants.…”

Chemical phenotype as important and dynamic niche dimension of plants

“…Chemodiversity can change with domestication: for example, leaves of domesticated alfalfa show a higher saponin richness but a lower variability in saponin composition than the wild relatives (Robinson et al ., 2020). However, for domestication, plants with a high chemodiversity are becoming increasingly relevant, as they may be better protected against diseases (Espinosa‐García et al ., 2021). In conclusion, we need to simultaneously consider the mosaic of different niche realisation processes for a comprehensive understanding of eco‐evolutionary dynamics and ecosystem processes.…”

The role of phytochemical diversity in the management of agroecosystems

“…The level of plant resistance to pests and pathogens has been related to the heterogeneity of the dynamic mosaic composition of structural, functional, and nutritional phytochemical diversity , Glassmire et al 2019. However, the homogeneity or heterogeneity in phytochemical diversity in terms of resistance will depend on the specific pest or pathogen (Espinosa-García et al 2021). For example, heterogeneity for a generalist consumer, such as Phytophthora cinnamomi, which can attack about 5,000 plant species belonging to more than 40 families (Hardham & Blackman 2018), will be different from that of a specialist such as the Abert's squirrel, which discriminates the chemotypes of pine trees of the same species when feeding on them (Snyder 1992).…”

“…Nevertheless, the random addition of plant secondary metabolites to a mixture does not assure its efficacy because antagonist interactions among the PSM may occur, and the plant consumers may detoxify that mixture (Whitehead et al 2021). Likewise, the sole addition of new phytochemical variants in a population does not imply increased stability or resistance against the local assemblage of consumers for the same reasons that may operate at the mixture scale (Espinosa-García et al 2021). Thus, the novel phytochemical combinations must undergo natural selection, leaving the combinations that add up to the plants' fitness or the population's persistence.…”