Genetic analyses of nickel tolerance in a North American serpentine endemic plant, Caulanthus amplexicaulis var. barbarae (Brassicaceae)

Our plain-English summary of Genetic analyses of nickel tolerance in a North American serpentine endemic plant, Caulanthus amplexicaulis var. barbarae (Brassicaceae), by A.M. Burrell, A.K. Hawkins, A.E. Pepper (American Journal of Botany, 2012).

The study

• Authors: A.M. Burrell, A.K. Hawkins, A.E. Pepper
• Journal: American Journal of Botany
• Published: 2012;99(11):1875-83
• Cited by: 9 articles, as counted by NIH iCite
• Read it: PubMed · Publisher

Abstract

Premise Of The Study: The evolution of metal tolerance in plants is an important model for studies of adaptation to environment, population genetics, and speciation. Here, we investigated nickel tolerance in the North American serpentine endemic Caulanthus amplexicaulis var. barbarae in comparison with its nonserpentine sister taxon C. amplexicaulis var. amplexicaulis. We hypothesized that the serpentine endemic would have a heritable growth advantage on nickel-containing substrates.

Methods: We employed an artificial growth assay to quantify biomass accumulation. Study plants were crossed to create an F(2:3) population that was used to determine the heritability of nickel tolerance and to map quantitative trait loci (QTL). Nickel accumulation in both laboratory populations and native specimens was examined using energy-dispersive x-ray fluorescence (EDXRF).

Key Results: The serpentine endemic had a dramatic growth advantage at concentrations of nickel >30 µmol/L. Caulanthus amplexicaulis var. barbarae and its nonserpentine sister taxon both accumulated nickel to substantial levels. Nickel tolerance was highly heritable (h(2) = 0.59) and not associated with accumulation. The QTL analyses identified two major loci for nickel tolerance, on linkage group 2 (LG2) and linkage group 9 (LG9).

Conclusions: In our study, nickel tolerance was determined by two major loci with large effects. At both loci, alleles from the serpentine parent conferred positive effects on nickel tolerance, suggesting that they are adaptive in the natural serpentine environment. The mechanism of nickel tolerance in the serpentine plant was not exclusion of nickel. Nickel tolerance may have an inducible component in C. amplexicaulis var. barbarae.

In plain English

This laboratory study concerned plants and nickel. It did not study asbestos or human health. The authors compared two closely related varieties of a southern California plant: Caulanthus amplexicaulis var. barbarae, a strict serpentine-soil endemic, and var. amplexicaulis, found largely on granitic soils. Inbred plants were grown in sand watered with nutrient solution containing 0 to 1000 µmol/L nickel chloride, and above-ground dry mass was weighed after 32 days. Nickel at 200 µmol/L killed the non-serpentine line, while the serpentine line showed only modestly reduced growth. In 88 families bred from a cross of the two lines and grown at 80 µmol/L nickel, tolerance had an estimated heritability of 0.59. Two genetic regions, on linkage groups 2 and 9, were linked to tolerance, and at both the serpentine parent's version increased growth. Both varieties accumulated substantial nickel in their leaves. In the crossed families, tolerance showed no correlation with the amount of nickel accumulated in plant tissue. The authors concluded that nickel tolerance was determined by two major loci with large effects and was not achieved by excluding nickel.

We wrote this plain-English summary from the full article with the help of AI, and a second AI model checked each sentence against the article. It is not the authors' wording; the abstract and the article are their own account.

What the study did and found

• Design: Laboratory plant genetics experiment: growth assays of two inbred parental lines in chemically defined sand culture with added nickel, then heritability estimation and quantitative trait locus (QTL) mapping in families from a cross between them, plus nickel measurement in leaves
• Who was studied: Plants, not people. Inbred lines of Caulanthus amplexicaulis var. amplexicaulis (CAA1, non-serpentine) and var. barbarae (CAB1, serpentine endemic), with 40 seeds per variety per treatment. Also 88 F3 families from a CAA1 by CAB1 cross, with nine plants per family. Also three wild CAB plants and their soils from a serpentine outcrop near Figueroa Mountain, California
• Exposure: Nickel chloride added to quarter-strength Murashige and Skoog nutrient medium at 0, 30, 60, 80, 100, 200, 500 or 1000 µmol/L. No asbestos or fibers were studied
• Main results:
  • Nickel at 200 µmol/L was completely lethal to the non-serpentine line CAA1
  • The serpentine line CAB1 had only modestly reduced biomass with increasing nickel and no other signs of nickel toxicity up to 1000 µmol/L
  • CAB1 biomass rose from 6.25 plus or minus 1.83 mg/plant dry mass at 500 µmol/L to 10.5 plus or minus 1.45 mg/plant at 1000 µmol/L nickel
  • In the F3 families grown at 80 µmol/L nickel, heritability of nickel tolerance was estimated at h2 = 0.59 (N = 378 samples)
  • Two QTL exceeded the genome-wide significance threshold (LOD 3.9): LOD 6.6 on linkage group 2 and 6.4 on linkage group 9 by composite interval mapping (4.7 and 4.6 by inclusive composite interval mapping)
  • By inclusive composite interval mapping, the two QTL explained 28% and 26% of total phenotypic variance
  • At both QTL, alleles from the serpentine parent (CAB) were associated with greater biomass
  • When the same families were grown without added nickel, no growth differences could be attributed to these genomic regions
  • Both lines accumulated substantial nickel in their uppermost leaves. CAA1 accumulated slightly more than CAB1 in all comparable conditions, but the difference was statistically significant only at 60 µmol/L (P = 0.043)
  • In the F2:3 families, tissue nickel concentration showed no correlation with nickel tolerance (biomass), with or without outliers
  • CAB1's tolerance in the laboratory was not achieved by excluding nickel. CAB1 at 1 mmol/L accumulated up to nearly 1% of dry mass as nickel
  • In three wild CAB plants on a serpentine outcrop, tissue nickel (N = 10 samples) ranged from 10.4 to 252 µg/g dry mass, mean 101 µg/g. Nearby soil averaged 1537 plus or minus 181 µg/g nickel
• The authors' conclusion: The authors concluded that nickel tolerance was determined by two major loci with large effects. Because serpentine-parent alleles had positive effects at both loci, they suggested these alleles are adaptive on serpentine. They also suggested tolerance may have an inducible component in var. barbarae
• Limitations the authors state:
  • The authors noted a relatively small mapping population (88 F2:3 families) and therefore also used a mapping method less sensitive to small-population biases

Topics

The National Library of Medicine indexes this study under subjects our site covers: Chrysotile.

Medical terms in this study, explained in our Lexicon: Serpentine Group, Endemic.

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