Research Article: Possible mechanisms of pollination failure in hybrid carrot seed and implications for industry in a changing climate

Date Published: June 30, 2017

Publisher: Public Library of Science

Author(s): Melissa Ann Broussard, Flore Mas, Brad Howlett, David Pattemore, Jason M. Tylianakis, William Oki Wong.

http://doi.org/10.1371/journal.pone.0180215

Abstract

Approximately one-third of our food globally comes from insect-pollinated crops. The dependence on pollinators has been linked to yield instability, which could potentially become worse in a changing climate. Insect-pollinated crops produced via hybrid breeding (20% of fruit and vegetable production globally) are especially at risk as they are even more reliant on pollinators than open-pollinated plants. We already observe a wide range of fruit and seed yields between different cultivars of the same crop species, and it is unknown how existing variation will be affected in a changing climate. In this study, we examined how three hybrid carrot varieties with differential performance in the field responded to three temperature regimes (cooler than the historical average, average, and warmer that the historical average). We tested how temperature affected the plants’ ability to set seed (seed set, pollen viability) as well as attract pollinators (nectar composition, floral volatiles). We found that there were significant intrinsic differences in nectar phenolics, pollen viability, and seed set between the carrot varieties, and that higher temperatures did not exaggerate those differences. However, elevated temperature did negatively affect several characteristics relating to the attraction and reward of pollinators (lower volatile production and higher nectar sugar concentration) across all varieties, which may decrease the attractiveness of this already pollinator-limited crop. Given existing predictions of lower pollinator populations in a warmer climate, reduced attractiveness would add yet another challenge to future food production.

Partial Text

Insect-pollinated crops comprise approximately one-third of the global food supply [1]. Many of these plants owe their present uniformity [2], disease resistance [2], and high yields [3–6] to hybrid production systems, including carrot, tomato, onion, melons, squash, brassicas, and eggplant [7]—together totaling nearly 20% of global crop production [8]. Because these production systems rely on crossing two parent lines, one of which is rendered male-sterile by hand-emasculation or genetic techniques, they are even more reliant on insect pollinators than their open-pollinated counterparts, do not require insects to cross from one parent line to the other [9–12]. Global reports of declines in many pollinator communities [13; 14], changing climate shifting pollinating insects’ active time away from peak bloom [15], and that pollinator reliance has been linked with reduced yield stability [16], indicate that hybrid systems may be at greater risk from additional disturbances than open-pollinated systems.

This study was conducted in New Zealand as it is one of the world’s largest producers of carrot seed [39]. We exposed carrot (Daucus carota L) plants to experimental temperature treatments, and measured characteristics relating to their innate ability to produce seed (‘Plant Fertility Metrics’, below) as well as several metrics that may affect their attractiveness to pollinators in the field (‘Plant Attractiveness Metrics’, below). To assess the extent to which these characters contribute to differences in yield and how they may respond to climate warming, we examined the correlations between each one and plant variety, temperature, and time-of-day in generalized linear mixed-effects models (GLMMs), generalized additive mixed-effects models (GAMMs) or ordination-based tests.

We found numerous effects of plant variety, temperature, and time-of-day on measures of both plant fertility and attractiveness to pollinators (see Fig 2 for a summary).

While environmental conditions at flowering time affected some plant fertility and attractiveness measures, we did not find any interaction effects between plant variety and temperature. This implies that the differences observed between the poor-, medium-, and excellent-performing carrots were due largely to innate plant characteristics (Fig 2), which did not respond to temperature. Our data suggest numerous mechanisms of poor performance in the field, as the ‘poor’ variety consistently underperformed the other two: it bloomed late, 50% of the male-fertile plants failed to even initiate flowering, had the worst synchronization between male-sterile and male-fertile lines (Fig 3), relatively low seed set (Fig 4), and pollen viability typically below 20% (Fig 5). Additionally, the nectar phenolic profiles showed a wide gap between the varieties. The poor line’s nectar was high in coumaric acid, which has been found to upregulate bee detoxification pathways [61], and ferulic acid (Fig 7), which, while commonly found in honey bee propolis [62], is thought to be an insect feeding deterrent [63]. Similarly, the poor line is low in caffeic acid, which is highly attractive to bees at modest concentrations [64].

 

Source:

http://doi.org/10.1371/journal.pone.0180215

 

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