Resistance and Tolerance to Root Herbivory in Maize Were Mediated by Domestication, Spread, and Breeding

Abstract

Plants may defend against herbivory and disease through various means. Plant defensive strategies against herbivores include resistance and tolerance, which may have metabolic costs that affect plant growth and reproduction. Thus, expression of these strategies may be mediated by a variety of factors, such as resource availability, herbivory pressure, and plant genetic variation, among others. Additionally, artificial selection by farmers and systematic breeding by scientists may mediate the expression of resistance and tolerance in crop plants. In this study, we tested whether maize defense against Western corn rootworm (WCR) was mediated by the crop's domestication, spread, and modern breeding. We expected to find a trend of decreasing resistance to WCR with maize domestication, spread, and breeding, and a trend of increasing tolerance with decreasing resistance. To test our expectations, we compared resistance and tolerance among four Zea plants spanning those processes: Balsas teosinte, Mexican landrace maize, US landrace maize, and US inbred maize. We measured the performance of WCR larvae as a proxy for plant resistance, and plant growth as affected by WCR feeding as a proxy for plant tolerance. Our results showed that domestication and spread decreased maize resistance to WCR, as expected, whereas breeding increased maize resistance to WCR, contrary to expected. Our results also showed that maize resistance and tolerance to WCR are negatively correlated, as expected. We discussed our findings in relation to ecological-evolutionary hypotheses seeking to explain defense strategy evolution in the contexts of plant resistance-productivity trade-offs, plant tolerance-resistance trade-offs, and varying resource availability vis-à-vis plant physiological stress and herbivory pressure. Finally, we suggested that defense strategy evolution in maize, from domestication to the present, is predicted by those ecological-evolutionary hypotheses.

Maize Biochemical Defences against a Rootworm Were Mediated by Domestication, Spread, and Breeding

“…While previous studies showed that 10-OPEA increased in maize roots 7 days after WCR feeding, which was correlated with increases in LOX3 and other 9-LOXs [68], our data suggests that, relative to the maizes, BTEO can more readily activate this sub-branch of the 9-LOX pathway in response to WCR feeding. Coincident with this study's results, our previous study showed that BTEO was more resistant but less tolerant to WCR than MXLR and maizes generally [51]. Put together, this and our prior study's results suggest that the stronger resistance and weaker tolerance to WCR in BTEO compared to MXLR is likely due to elevated levels of induced jasmonates and low levels of IAA in BTEO, while defence in MXLR, and maize generally, is due to high constitutive levels of 9-oxylipins and IAA.…”

“…Prior studies showed that landrace maizes are planted on ~80% of the area devoted to maize in Mexico, encompassing mostly hillsides with poor soils, while improved commercial varieties are planted on the remaining ~20% of the area, and that farmers will plant commercial varieties on good soils and landraces on poorer soils, when they have a choice [73][74][75][76][77]. Finally, while US landraces (no longer planted commercially) and inbred lines were developed for the same environments, the availability of major soil nutrients, e.g., nitrogen, differed greatly between the early and late portions of the 20 th century, associated with intensification of maize production reliant on commercial (hybrid) varieties and other inputs (e.g., fertilizers and insecticides to support high crop productivity and offset insect injury) that began in the middle of that century [50,51,78,79]. For example, prior to the 1930s, few maize growers employed fertilizers because they were uneconomical or unavailable, while the use of synthetic nitrogen fertilizers nearly tripled between 1964 and 1985 [78][79][80].…”

“…Such may be the case for maize (Zea mays mays L.), which was cultivated in increasingly favourable contexts, and underwent successive bouts of natural and artificial selection, as it was domesticated, spread in the Americas and became a dietary staple, and, most recently, whilst subjected to systematic breeding for enhanced yield under intensive agriculture [17,41,[46][47][48][49]. Indeed, prior studies showed that these processes significantly shaped how maize responds to herbivory [47,50,51].…”

“…In addition to domestication, spread, and breeding, previous studies suggested that herbivory pressure, resource availability, and agricultural intensification may mediate the evolution of maize defences against herbivores, including Western corn rootworm (WCR) (Diabrotica virgifera virgifera LeConte) [50,51]. As for other crops and herbivores, herbivory pressure by WCR likely contributed to shaping maize defensive strategies, whether based on resistance or tolerance, after the crop spread from central Mexico to North America [37,[51][52][53]. Maize resistance (e.g., antibiosis) and tolerance (e.g., compensatory growth) to WCR depend on the triggering of signalling cues, particularly phytohormones.…”

“…Particularly, resistance may imply synthesis of secondary metabolites triggered by changes in phytohormone levels, whereas tolerance may depend in part on synthesis of growth-related phytohormones [6,12,20]. Thus, constitutive and herbivoreinduced phytohormone profiles relevant to maize resistance and tolerance to WCR, and other herbivores, may have been mediated by the crop's domestication, spread, and systematic breeding, as well as by variable herbivory pressure, resource availability, and agricultural intensification [50,51,54].…”