Are All Clonal Crops Equally Vulnerable To Insect Pest Attacks? The Avocado File

In wild populations, most plant species exhibit high genetic diversity, which often is manifested as high chemical diversity and variation. This chemical heterogeneity is very important in plant populations to resist insect and pathogen attack. However, in monoculture crops, where chemical diversity in quality and quantity is low, possibilities to resist pest attack and diseases are diminished.

It is common knowledge that genetic uniformity in annual crops leads to disastrous pest and/or pathogen attack. An emblematic example of this phenomenon is the relationship between wheat and stem rust (Puccinia graminis f.sp. tritici) where resistance genes in uniform wheat varieties were overcome by the stem rust in a few years. The epidemic caused by stem rust was answered by humans developing new wheat varieties that again favored new devastating stem rust strains.

In clonal crops, such as potatoes, avocados, bananas, apples, grapes and strawberries, genetic and chemical diversity are minimized in order to maintain yield and desirable agronomic and organoleptic characteristics. The genetic uniformity in clonal crops was one of the main causes of agro-alimentary catastrophes such as the Irish potato famine in 1845-1849. If we already know that uniformity in crops is a recipe for disaster and that variability is the antidote, how is it that clonal crops still thrive in modern agriculture, even in the organic one?

Plants produce thousands of secondary compounds (a.k.a phytochemicals) that are present as mixtures in plant tissues. Variation in concentration and composition of these mixtures can affect, positive or negatively, herbivorous insect performance (survival, foraging, feeding, oviposition, growth, weight, fertility, etc.). While some mixtures or specific compounds affect negatively growth or weight gain in generalist insects, these same compounds may be beneficial for specialist insects acting as oviposition stimulants.

The Hass avocado is a clonal crop, propagated by grafting. México harbors the biggest extension of avocado cropland, 166,000 ha, planted mainly with the cultivar Hass. The avocado tree is attacked by Copturus aguacatae, a branch-boring weevil that causes breakage of fruit-bearing branches. This weevil is endemic to Mexico and is a specialist insect that feeds only on varieties of avocados. Nowadays, it is one of the worst avocado pests because it limits fruit exportation and is potentially an invasive pest. Our team demonstrated that in the 1990s, Hass avocado orchards harbored three to thirteen tree chemotypes based on leaf terpenoids and phenylpropanoids. However, with the rapid expansion of the avocado crop, we recently detected orchards with just one tree chemotype. Is that chemical variation enough to function as a resistance factor against a specialist insect? Or is the Hass avocado crop disarmed against Copturus aguacatae?

We observed that within several orchards, some avocado trees were severely infested (many branches bored) while some of their neighbor trees remained untouched (non-bored). We hypothesized that bored and non-bored avocado trees were chemically different and thus differentially infested by Copturus aguacatae. To identify which specific compounds within the hundreds of phytochemicals in the branch tissues were related with resistance against weevil infestation, we used metabolic profiling by gas chromatography coupled to mass spectrometry. This technique allows the simultaneous analysis of a great number of compounds.

We sampled more than one hundred avocado trees in seven orchards in two seasons (rainy and dry), obtaining 210 chromatographic peaks. Contrary to our expectations, one leaf chemotype predominated in the orchards, suggesting that high phytochemical homogeneity within and among orchards prevailed. We found variation in branch phytochemistry between the rainy and dry seasons that obscured the differences between bored and non-bored trees. After controlling seasonal variation, we found many compounds differing between bored and non-bored trees; at that point, it was impossible to distinguish which compounds increased or decreased in response to insect attack and which ones were constitutive.

To resolve this quagmire, we compared the chemical composition of bored and non-bored branches from the same tree. We identified a group of sixteen compounds that increased in bored trees as a response to larvae feeding. Then, aside from that set of induced compounds, we identified constitutive obtusilactone A and α-humulene in high concentration on non-bored trees. These results suggest that both compounds are involved in Hass avocado tree resistance to weevil attack, probably acting as deterrents.

In summary, we found several sources that maintain phytochemical variation between and within avocado clones, identifying what compounds are correlated to resistance and induced response to insect attacks. The next step is to test whether these compounds have the expected effect on the insect. In general terms, we showed that a clonal crop exhibits constitutive and induced phytochemical variation related to pest resistance. Moreover, even among individual branches of the same clone, different suites of phytochemicals are deployed as something similar to the “moving target to herbivores” posed by Adler and Karban (Am. Nat., 144 (1994), pp. 813-832).

Perennial crops, such as the Hass avocado tree, could be not so defenseless against insect pests in comparison to annual crops. We found additional sources of phytochemical variation in an apparently homogenous crop that probably constitutes a resistance trait against a specialist insect that faces a changing clonal host.