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      Crop Domestication Alters Floral Reward Chemistry With Potential Consequences for Pollinator Health

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          Abstract

          Crop domestication can lead to weakened expression of plant defences, with repercussions for herbivore and pathogen susceptibility. However, little is known about how domestication alters traits that mediate other important ecological interactions in crops, such as pollination. Secondary metabolites, which underpin many defence responses in plants, also occur widely in nectar and pollen and influence plant-pollinator interactions. Thus, domestication may also affect secondary compounds in floral rewards, with potential consequences for pollinators. To test this hypothesis, we chemically analysed nectar and pollen from wild and cultivated plants of highbush blueberry ( Vaccinium corymbosum L.), before conducting an artificial diet bioassay to examine pollinator-pathogen interactions. Our results indicated that domestication has significantly altered the chemical composition of V. corymbosum nectar and pollen, and reduced pollen chemical diversity in cultivated plants. Of 20 plant metabolites identified in floral rewards, 13 differed significantly between wild and cultivated plants, with a majority showing positive associations with wild compared to cultivated plants. These included the amino acid phenylalanine (4.5 times higher in wild nectar, 11 times higher in wild pollen), a known bee phagostimulant and essential nutrient; and the antimicrobial caffeic acid ester 4- O-caffeoylshikimic acid (two times higher in wild nectar). We assessed the possible biological relevance of variation in caffeic acid esters in bioassays, using the commercially available 3- O-caffeoylquinic acid. This compound reduced Bombus impatiens infection by a prominent gut pathogen ( Crithidia) at concentrations that occurred in wild but not cultivated plants, suggesting that domestication may influence floral traits with consequences for bee health. Appreciable levels of genetic variation and heritability were found for most floral reward chemical traits, indicating good potential for selective breeding. Our study provides the first assessment of plant domestication effects on floral reward chemistry and its potential repercussions for pollinator health. Given the central importance of pollinators for agriculture, we discuss the need to extend such investigations to pollinator-dependent crops more generally and elaborate on future research directions to ascertain wider trends, consequences for pollinators, mechanisms, and breeding solutions.

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          Most cited references102

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          rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models

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            Recruitment of entomopathogenic nematodes by insect-damaged maize roots.

            Plants under attack by arthropod herbivores often emit volatile compounds from their leaves that attract natural enemies of the herbivores. Here we report the first identification of an insect-induced belowground plant signal, (E)-beta-caryophyllene, which strongly attracts an entomopathogenic nematode. Maize roots release this sesquiterpene in response to feeding by larvae of the beetle Diabrotica virgifera virgifera, a maize pest that is currently invading Europe. Most North American maize lines do not release (E)-beta-caryophyllene, whereas European lines and the wild maize ancestor, teosinte, readily do so in response to D. v. virgifera attack. This difference was consistent with striking differences in the attractiveness of representative lines in the laboratory. Field experiments showed a fivefold higher nematode infection rate of D. v. virgifera larvae on a maize variety that produces the signal than on a variety that does not, whereas spiking the soil near the latter variety with authentic (E)-beta-caryophyllene decreased the emergence of adult D. v. virgifera to less than half. North American maize lines must have lost the signal during the breeding process. Development of new varieties that release the attractant in adequate amounts should help enhance the efficacy of nematodes as biological control agents against root pests like D. v. virgifera.
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              Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops.

              Domesticated food crops are derived from a phylogenetically diverse assemblage of wild ancestors through artificial selection for different traits. Our understanding of domestication, however, is based upon a subset of well-studied 'model' crops, many of them from the Poaceae family. Here, we investigate domestication traits and theories using a broader range of crops. We reviewed domestication information (e.g. center of domestication, plant traits, wild ancestors, domestication dates, domestication traits, early and current uses) for 203 major and minor food crops. Compiled data were used to test classic and contemporary theories in crop domestication. Many typical features of domestication associated with model crops, including changes in ploidy level, loss of shattering, multiple origins, and domestication outside the native range, are less common within this broader dataset. In addition, there are strong spatial and temporal trends in our dataset. The overall time required to domesticate a species has decreased since the earliest domestication events. The frequencies of some domestication syndrome traits (e.g. nonshattering) have decreased over time, while others (e.g. changes to secondary metabolites) have increased. We discuss the influences of the ecological, evolutionary, cultural and technological factors that make domestication a dynamic and ongoing process. © 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                26 September 2018
                2018
                : 9
                : 1357
                Affiliations
                [1] 1Department of Plant Protection Biology, Swedish University of Agricultural Sciences , Alnarp, Sweden
                [2] 2Department of Biology, University of Massachusetts Amherst , Amherst, MA, United States
                [3] 3Department of Applied Ecology, North Carolina State University , Raleigh, NC, United States
                [4] 4Royal Botanic Gardens , Kew, Richmond, United Kingdom
                [5] 5Natural Resources Institute, University of Greenwich , London, United Kingdom
                Author notes

                Edited by: Clay Carter, University of Minnesota Twin Cities, United States

                Reviewed by: Neelendra K. Joshi, University of Arkansas, United States; Kevin Davies, The New Zealand Institute for Plant &Food Research Ltd., New Zealand

                *Correspondence: Paul A. Egan, paul.egan@ 123456slu.se

                Present address: Evan C. Palmer-Young, Department of Entomology, University of California, Riverside, Riverside, CA, United States

                This article was submitted to Functional Plant Ecology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.01357
                6169423
                30319666
                c6cb39ed-5d3d-47dd-99e0-3dd3bedd4870
                Copyright © 2018 Egan, Adler, Irwin, Farrell, Palmer-Young and Stevenson.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 27 April 2018
                : 28 August 2018
                Page count
                Figures: 4, Tables: 2, Equations: 0, References: 120, Pages: 14, Words: 0
                Funding
                Funded by: Division of Environmental Biology 10.13039/100000155
                Award ID: 1258096
                Award ID: 1256817
                Award ID: 1638866
                Funded by: U.S. Department of Agriculture 10.13039/100000199
                Award ID: USDA-AFRI 2013-02536
                Award ID: 2016-67011-24698
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                domestication,floral rewards,vaccinium,crop evolution,pollinator-pathogen interactions,bombus impatiens,pollinator health,phytochemicals

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