Plasticity and evolution in drought avoidance and escape in the annual plant Brassica rapa

Department of Biology, Fordham University, 160 Larkin Hall, 441 E. Fordham Road, Bronx, NY 10458, USA.
New Phytologist (Impact Factor: 7.67). 04/2011; 190(1). DOI: 10.1111/j.1469-8137.2010.03603.x
Source: PubMed


• A key question in ecological genetics is to what extent do plants adapt to changes in climatic conditions, such as drought, through plasticity or evolution. • To address this question, seeds of 140 maternal families of Brassica rapa were generated from collections made before (1997) and after (2004) a natural drought. These seeds were planted in the glasshouse and grown under low-water and high-water conditions. • Post-drought lines flowered earlier than pre-drought lines, showing an evolutionary shift to earlier flowering. There was significant genetic variation and genotype by environment (G × E) interactions in flowering time, indicating genetic variation in plasticity in this trait. Plants that flowered earlier had fewer leaf nodes and lower instantaneous (A/g) and integrated (δ(13) C) water use efficiency than late-flowering plants. • These results suggest that B. rapa plants escape drought through early flowering rather than avoid drought through increased water use efficiency. The mechanism of this response appears to be high transpiration and inefficient water use, leading to rapid development. These findings demonstrate a trade-off between drought avoidance and escape, and indicate that, in this system, where drought acts to shorten the growing season, selection for drought escape through earlier flowering is more important than phenotypic plasticity.

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Available from: Steven Joseph Franks, Mar 17, 2014
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    • "this adaptive evolutionary change may have ecological effects by exploring plant susceptibility to a fungal pathogen. Altered susceptibility is particularly likely because the early flowering plants, which are able to escape drought, allocate resources to rapid growth and development (Franks 2011), potentially leaving fewer resources available for defense. We hypothesized that postdrought descendant plants would show greater disease susceptibility than predrought ancestral plants, with the drought causing the evolution of increased susceptibility as a byproduct of selection for earlier flowering. "
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    ABSTRACT: Recent studies have demonstrated adaptive evolutionary responses to climate change, but little is known about how these responses may influence ecological interactions with other organisms, including natural enemies. We used a resurrection experiment in the greenhouse to examine the effect of evolutionary responses to drought on the susceptibility of Brassica rapa plants to a fungal pathogen, Alternaria brassicae. In agreement with previous studies in this population, we found an evolutionary shift to earlier flowering post-drought, which was previously shown to be adaptive. Here we report the novel finding that post-drought descendant plants were also more susceptible to disease, indicating a rapid evolutionary shift to increased susceptibility. This was accompanied by an evolutionary shift to increased specific leaf area (thinner leaves) following drought. We found that flowering time and disease susceptibility displayed plastic responses to experimental drought treatments, but that this plasticity did not match the direction of evolution, indicating that plastic and evolutionary responses to changes in climate can be opposed. The observed evolutionary shift to increased disease susceptibility accompanying adaptation to drought provides evidence that even if populations can rapidly adapt in response to climate change, evolution in other traits may have ecological effects that could make species more vulnerable. This article is protected by copyright. All rights reserved.
    Full-text · Article · Dec 2015 · Evolution
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    • "Flowering time was shown to be heritable, so variation in this trait has some genetic basis (Franks, Sim & Weis, 2007). Subsequent work showed that early flowering plants have lower water use efficiency and flower at a smaller size and earlier developmental stage (Franks, 2011). However, the genetic basis of this rapid evolutionary change in flowering time, as well as the genetic basis of flowering time variation within populations, remained unknown. "
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    ABSTRACT: Understanding the genetic basis of natural phenotypic variation is of great importance, particularly since selection can act on this variation to cause evolution. We examined expression and allelic variation in candidate flowering time loci in Brassica rapa plants derived from a natural population and showing a broad range in the timing of first flowering. The loci of interest were orthologs of the Arabidopsis genes FLC and SOC1 ( BrFLC and BrSOC1 , respectively), which in Arabidopsis play a central role in the flowering time regulatory network, with FLC repressing and SOC1 promoting flowering. In B. rapa , there are four copies of FLC and three of SOC1 . Plants were grown in controlled conditions in the lab. Comparisons were made between plants that flowered the earliest and latest, with the difference in average flowering time between these groups ∼30 days. As expected, we found that total expression of BrSOC1 paralogs was significantly greater in early than in late flowering plants. Paralog-specific primers showed that expression was greater in early flowering plants in the BrSOC1 paralogs Br004928, Br00393 and Br009324 , although the difference was not significant in Br009324 . Thus expression of at least 2 of the 3 BrSOC1 orthologs is consistent with their predicted role in flowering time in this natural population. Sequences of the promoter regions of the BrSOC1 orthologs were variable, but there was no association between allelic variation at these loci and flowering time variation. For the BrFLC orthologs, expression varied over time, but did not differ between the early and late flowering plants. The coding regions, promoter regions and introns of these genes were generally invariant. Thus the BrFLC orthologs do not appear to influence flowering time in this population. Overall, the results suggest that even for a trait like flowering time that is controlled by a very well described genetic regulatory network, understanding the underlying genetic basis of natural variation in such a quantitative trait is challenging.
    Full-text · Article · Nov 2015 · PeerJ
    • "Disproportionately large flowers therefore might further raise water costs. Under drought, plants produce smaller flowers and smaller reproductive structures in general (Mal and Lovett-Doust 2005; Caruso 2006), and were also found to advance flowering phenology as a plastic as well as an evolutionary response (Dunne et al. 2003; Franks 2011). Precipitation is very variable across the European Alps as a result of the interplay of climatic patterns with the obstructing effect of mountain ranges. "
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    ABSTRACT: The timing of and relative investment in reproductive events are crucial fitness determinants for alpine plants, which have limited opportunities for reproduction in the cold and short growing seasons at high elevations. We use the alpine Anthyllis vulneraria to study whether flowering phenology and reproductive allocation have been under diversifying selection, and to assess genetic diversity and plastic responses to drought in these traits. Open-pollinated maternal families from three populations in each of two regions from the Swiss Alps with contrasting precipitation were grown in low and high soil moisture in a common garden. We measured onset, peak, and end of flowering, as well as vegetative and reproductive aboveground biomass. Population differentiation for each character (QST) was compared to differentiation at neutral microsatellite loci (FST) to test for past selection. We found population differentiation in onset and peak of flowering which results from natural selection according to QST–FST. End of flowering and biomass were not significantly differentiated among populations. Reduced soil moisture had no consistent effect on mean onset of flowering, and advanced peak and end of flowering by less than 1 week. Reproductive biomass was strongly decreased by lowered soil moisture. No genetic variation within or among populations was found for plasticity in any trait measured. The results suggest past heterogeneous selection on onset and peak of flowering in alpine Anthyllis vulneraria and potentially indicate local adaptation to differences in snowmelt date over distances <5 km. Limited variation in plastic responses to reduced soil moisture suggests that soil moisture might not vary between populations.
    No preview · Article · Sep 2015 · Alpine Botany
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