Variation in nickel accumulation in leaves, reproductive organs and floral rewards in two hyperaccumulating Brassicaceae species
- 491 Downloads
Metal hyperaccumulation by plants involves the uptake and sequestration of extremely high concentrations of soil heavy metals. It is unclear, however, whether plants that hyperaccumulate heavy metals do so across all organs, including reproductive ones, and whether floral metal accumulation varies depending on whether plants require pollinator visitation for reproduction.
We grew two species of nickel hyperaccumulators, one that requires pollinator visitation and the other an autonomous selfer, in two soil treatments: (1) control or (2) nickel-supplemented. We quantified nickel concentration in leaves, reproductive organs and floral rewards (pistils, anthers, pollen and nectar).
Nickel accumulated into all organs, with the autonomously selfing species (Noccaea fendleri subsp. glauca) accumulating higher concentrations, especially in anthers and pistils. Streptanthus polygaloides incorporated nickel into nectar, but at lower concentrations than floral organs. Both species incorporated nickel into pollen.
Nickel-hyperaccumulators incorporated nickel into all reproductive organs as well as rewards, suggesting possible reproductive consequences that may either be positive (e.g., elemental defense) or detrimental (e.g., reducing gamete viability or pollinator visitation) to plant fitness. Our work suggests that identifying any adaptive value of metal hyperaccumulation requires further study of floral metal accumulation and the reproductive consequences of metals in reproductive organs and rewards.
KeywordsNickel Metal hyperaccumulation Brassicaceae Flowers Streptanthus polygaloides Noccaea fendleri subsp. glauca
K. DeHart and C. Murray assisted with plant organ/reward analysis, E. York and K. Schuller provided greenhouse assistance, G. Arceo-Gomez, M. Koski and the Ashman lab and two anonymous reviewers provided useful comments on the research and/or manuscript. This research was funded by a Botany In Action Fellowship from the Phipps Conservatory and Botanical Gardens, an Ivy McManus Diversity Fellowship (University of Pittsburgh) and an Andrew Mellon Predoctoral Fellowship (University of Pittsburgh) to GAM, NSF (EAR-IF 0948366) to DJB, and NSF (DEB 1020523, 1241006) to TLA.
- Al-Shehbaz IA (2013) Brassicaceae. In: Flora of North America Editorial Committee, eds. 1993+. Flora of North America north of Mexico. 16+ vols. New York and OxfordGoogle Scholar
- Baker I (1979) Methods for the determination of volumes and sugar concentrations from nectar spots on paper. Phytochem Bull 12:40–42Google Scholar
- Baldwin BG, Goldman DH, Keil DJ, Patterson R, Rosatti TJ, Wilken DH (eds) (2012) The Jepson manual: vascular plants of California. University of California Press, BerkeleyGoogle Scholar
- Boyd RS, Martens S (1992) The raison d’etre for metal hyperaccumulation by plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 279–289Google Scholar
- Brooks RR (1998) Phytochemistry of hyperaccumulators. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, New York, pp 15–53Google Scholar
- Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62:471–481. doi: 10.1016/S0031-9422(02)00549-6
- Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, NiwotGoogle Scholar
- Littell RC, Stroup WW, Freund RJ (2002) SAS for linear models. SAS Institute, CaryGoogle Scholar
- Marschner P (2012) Mineral nutrition of higher plants, 3rd edn. Academic, San DiegoGoogle Scholar
- Meindl GA, Bain DJ, Ashman T-L (2014) Nickel accumulation in leaves, floral organs and rewards varies by serpentine soil affinity. AoB Plants. doi: 10.1093/aobpla/plu036
- Quinn CF, Prins CN, Freeman JL, Gross AM, Hantzis LJ, Reynolds RJ, Yang S, Covey PA, Bañuelos GS, Pickering IJ, Fakra SC, Marcus MA, Arathi HS, Pilon-Smits EA (2011) Selenium accumulation in flowers and its effects on pollination. New Phytol 192:727–737. doi: 10.1111/j.1469-8137.2011.03832.x PubMedCrossRefGoogle Scholar
- Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel JL, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils. NATO Science Series: IV: earth and environmental sciences, vol 68. Springer, New York, pp 1–25Google Scholar
- Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: Using plants to clean up the environment. Wiley, New York, pp 193–229Google Scholar
- Safford HD, Viers JH, Harrison SP (2005) Serpentine endemism in the California flora: a database of serpentine affinity. Madroño 52: 222–257. doi: 10.3120/0024-9637(2005)52[222:SEITCF]2.0.CO;2
- SAS Insitute Inc. 2011. SAS/STAT 9.3 User’s Guide. SAS Institute Inc.Google Scholar
- Valdez Barillas JR, Quinn CF, Freeman JL, Lindblom SD, Fakra SC, Marcus MA, Gilligan TM, Alford ER, Wangeline AL, Pilon-Smits EA (2012) Selenium distribution and speciation in the hyperaccumulator Astragalus bisulcatus and associated ecological partners. Plant Physiol 159:1834–1844. doi: 10.1104/pp. 112.199307 PubMedCrossRefPubMedCentralGoogle Scholar
- Vogel-Mikuš K, Pongrac P, Kump P, Necemer M, Simcic J, Pelicon P, Budnar M, Povh B, Regvar M (2007) Localisation and quantification of elements within seeds of Cd/Zn hyperaccumulator Thlaspi praecox by micro-PIXE. Environ Poll 147:50-59. doi: 10.1016/j.envpol.2006.08.026 DOI: 10.1016/j.envpol.2006.08.026#doilink
- Wall MA, Boyd RS (2002) Nickel accumulation in serpentine arthropods from the Red Hills, California. Pan Pac Entomol 78:168–176Google Scholar