The genus Odontarrhena (Brassicaceae) in Albania: Taxonomy and Nickel accumulation in a critical group of metallophytes from a major serpentine hot-spot
Abstract:Metal hyperaccumulator plants represent a unique biological resource for scientific research and practical applications. Though essential, however, an adequate knowledge of the systematics of these plants is often missing. This is the case of Odontarrhena, a large but taxonomically critical group of nickel hyperaccumulators from Eurasia. We present a study on this genus in Albania, to fill a gap in our knowledge of this group from a major centre of diversity of metallicolous flora, and to contribute updated in… Show more
“…This confirms that most literature reports on Ni-accumulation ability in “ O. muralis ” are to be referred to closely related Ni-accumulating taxa that are widespread in the Balkans, such as O. chalcidica and O. decipiens (Nyár.) L.Cecchi and Selvi (Cecchi et al 2018 ; Bettarini et al 2019 ).…”
Section: Discussionmentioning
confidence: 99%
“…Accordingly, populations and plants of O. sibirica with contrasting levels of Ni in their shoots should be compared for their genetic traits as well, also looking at possible hybridization and introgression with other locally coexisting Ni accumulating species of Odontarrhena. Hybridization and genetic admixing are indeed known to occur between some sympatric Ni-accumulating species of this genus in similar habitats of the Balkans, especially in anthropogenic sites with heavy disturbance, and not always associated with detectable phenotypic traits in the plants (Cecchi et al 2018 ; Coppi et al 2020 in press). Though the two Turkish accumulating specimens that we examined did not show clear “hybrid signatures”, these were from heavily disturbed sites and growing near other congeneric Ni accumulators [ O. corsica (Duby) Španiel, Al-Shehbaz, D.A.German and Marhold, O. dudleyi (Adıgüzel and R.D.Reeves) Španiel, Al-Shehbaz, D.A.German and Marhold, and group of O. muralis ], which might have favoured interspecific gene flow and the origin of introgressive populations.…”
Section: Discussionmentioning
confidence: 99%
“…Endl. (see Cecchi et al 2018 ; Bettarini et al 2019 ), and the obligate Ni-hyperaccumulator O. smolikana (Nyár.) Španiel, Al-Shehbaz, D.A.German and Marhold subsp.…”
Main conclusion
Odontarrhena is a highly diverse genus of Ni-hyperaccumulators. Here, we demonstrate substantial inability to accumulate Ni in the facultative serpentinophyte O. sibirica, which seems a unique case among the numerous species of the genus that grow on ultramafic soils.
Abstract
Odontarrhena is the most diverse genus of Ni-accumulating plants in W Eurasia, with most taxa growing obligatorily or facultatively on ultramafic soils. A notable exception may be O. sibirica, a facultative serpentinophyte from the E Mediterranean and W Asia in which accumulation ability is still enigmatic. We addressed this issue using observational and experimental methods. Atomic Absorption Analysis of 33 herbarium specimens and plant and soil samples from seven ultramafic and non-ultramafic sites in Greece revealed shoot Ni values always much lower than 1000 µg g−1, non-significant differences between plants from the two soil types and no relationship with soil pH. Only two Turkish specimens from waste mines had shoot Ni concentration > 1000 µg g−1. The reasons for this deviating result remain obscure, but may be associated with inherent peculiarities of the local populations. When cultivated together with congeneric Ni-accumulating species on the same natural ultramafic soil, only O. sibirica was unable to accumulate the metal. Although plant growth was stimulated in hydroponics at relatively low NiSO4 levels (50–150 µM), as typical for hyperaccumulators, Ni-accumulation occurred only at higher concentrations which had a toxic effect. This peculiar combination of Ni-response traits could be the result of a partial evolutionary loss of ability with respect to all other Ni-accumulating congeneric species. For this, O. sibirica could represent a unique model system for further studies on the evolutionary dynamics, physiological mechanisms and genetic control of metal accumulation and homeostasis.
“…This confirms that most literature reports on Ni-accumulation ability in “ O. muralis ” are to be referred to closely related Ni-accumulating taxa that are widespread in the Balkans, such as O. chalcidica and O. decipiens (Nyár.) L.Cecchi and Selvi (Cecchi et al 2018 ; Bettarini et al 2019 ).…”
Section: Discussionmentioning
confidence: 99%
“…Accordingly, populations and plants of O. sibirica with contrasting levels of Ni in their shoots should be compared for their genetic traits as well, also looking at possible hybridization and introgression with other locally coexisting Ni accumulating species of Odontarrhena. Hybridization and genetic admixing are indeed known to occur between some sympatric Ni-accumulating species of this genus in similar habitats of the Balkans, especially in anthropogenic sites with heavy disturbance, and not always associated with detectable phenotypic traits in the plants (Cecchi et al 2018 ; Coppi et al 2020 in press). Though the two Turkish accumulating specimens that we examined did not show clear “hybrid signatures”, these were from heavily disturbed sites and growing near other congeneric Ni accumulators [ O. corsica (Duby) Španiel, Al-Shehbaz, D.A.German and Marhold, O. dudleyi (Adıgüzel and R.D.Reeves) Španiel, Al-Shehbaz, D.A.German and Marhold, and group of O. muralis ], which might have favoured interspecific gene flow and the origin of introgressive populations.…”
Section: Discussionmentioning
confidence: 99%
“…Endl. (see Cecchi et al 2018 ; Bettarini et al 2019 ), and the obligate Ni-hyperaccumulator O. smolikana (Nyár.) Španiel, Al-Shehbaz, D.A.German and Marhold subsp.…”
Main conclusion
Odontarrhena is a highly diverse genus of Ni-hyperaccumulators. Here, we demonstrate substantial inability to accumulate Ni in the facultative serpentinophyte O. sibirica, which seems a unique case among the numerous species of the genus that grow on ultramafic soils.
Abstract
Odontarrhena is the most diverse genus of Ni-accumulating plants in W Eurasia, with most taxa growing obligatorily or facultatively on ultramafic soils. A notable exception may be O. sibirica, a facultative serpentinophyte from the E Mediterranean and W Asia in which accumulation ability is still enigmatic. We addressed this issue using observational and experimental methods. Atomic Absorption Analysis of 33 herbarium specimens and plant and soil samples from seven ultramafic and non-ultramafic sites in Greece revealed shoot Ni values always much lower than 1000 µg g−1, non-significant differences between plants from the two soil types and no relationship with soil pH. Only two Turkish specimens from waste mines had shoot Ni concentration > 1000 µg g−1. The reasons for this deviating result remain obscure, but may be associated with inherent peculiarities of the local populations. When cultivated together with congeneric Ni-accumulating species on the same natural ultramafic soil, only O. sibirica was unable to accumulate the metal. Although plant growth was stimulated in hydroponics at relatively low NiSO4 levels (50–150 µM), as typical for hyperaccumulators, Ni-accumulation occurred only at higher concentrations which had a toxic effect. This peculiar combination of Ni-response traits could be the result of a partial evolutionary loss of ability with respect to all other Ni-accumulating congeneric species. For this, O. sibirica could represent a unique model system for further studies on the evolutionary dynamics, physiological mechanisms and genetic control of metal accumulation and homeostasis.
“…While the taxa from Greece are better understood, some of those from Albania, the former Yugoslav Republic of Macedonia (FYROM), and Bulgaria are still poorly known, preventing a correct estimation of the diversity of accumulators in the Balkans to be presented. A recent systematic revision of the genus in Albania (Cecchi et al, 2018) points to the existence of seven taxa, of which six Ni-hyperaccumulators are restricted to ultramafic soils (except for O. chalcidica, facultative serpentinophyte). A polyploid species of likely hybrid origin between O. chalcidica and O. smolikana, originally described from Mt.…”
Section: A Synthetic Overview Of Ni-hyperaccumulators In Europementioning
Ultramafic soils are typically enriched in nickel (Ni), chromium (Cr), and cobalt (Co) and deficient in essential nutrients, making them unattractive for traditional agriculture. Implementing agromining systems in ultramafic agricultural soils represent an ecological option for the sustainable management and re-valorisation of these low-productivity landscapes. These novel agroecosystems cultivate Ni-hyperaccumulating plants which are able to bioaccumulate this metal in their aerial plant parts; harvested biomass can be incinerated to produce Ni-enriched ash or "bio-ore" from which Ni metal, Ni ecocatalysts or pure Ni salts can be recovered. Nickel hyperaccumulation has been documented in ∼450 species, and in temperate latitudes these mainly belong to the family Brassicaceae and particularly to the genus Odontarrhena (syn. Alyssum pro parte). Agromining allows for sustainable metal recovery without causing the environmental impacts associated with conventional mining activities, and at the same time, can improve soil fertility and quality and provide essential ecosystem services. Parallel reductions in Ni phytotoxicity over time would also permit cultivation of conventional agricultural crops. Field studies in Europe have been restricted to Mediterranean areas and these only evaluated the Ni-hyperaccumulator Odontarrhena muralis s.l. Two recent EU projects (Agronickel and LIFE-Agromine) have established a network of agromining field sites in ultramafic regions with different edapho-climatic characteristics across Albania, Austria, Greece and Spain. Soil and crop management practices are being developed so as to Kidd et al. Sustainable Agromining Systems for Nickel Recovery optimize the Ni agromining process; field studies are evaluating the potential benefits of fertilization regimes, crop selection and cropping patterns, and bioaugmentation with plant-associated microorganisms. Hydrometallurgical processes are being up-scaled to produce nickel compounds and energy from hyperaccumulator biomass. Exploratory techno-economic assessment of Ni metal recovery by pyrometallurgical conversion of O. muralis s.l. shows promising results under the condition that heat released during incineration can be valorized in the vicinity of the processing facility.
“…scutarinum is to be excluded from the circumscription of O. bertolonii and included in that of the Balkan species O. chalcidica (Janka) Španiel, Al-Shehbaz, D.A. German & Marhold (Cecchi et al 2018). In 'Alyssum' bertolonii 'f.…”
Odontarrhena bertolonii is an endemic serpentine species of Tuscany and Liguria and a model system for nickel-hyperaccumulation research in plants. Phenotypic, genetic and karyological variability between populations was previously detected, but existence and distribution of cytotypes was unknown. Accordingly, we examined ploidy level in eight populations from the species range and tested the polyploid fitness hypothesis by analysing relationships with plant phenotype and seed germination capacity. Accessions from central-western Tuscany and Liguria resulted diploid, while those from the upper Tiber valley were tetraploid. Autopolyploidy via unreduced gametes is likely the mechanism for the origin of tetraploid plants. Size and mass were higher in tetraploid seeds, which germinated faster and to higher percentages than diploid ones. Tetraploid plants were more robust and taller, with more richly branched inflorescences. Silicle shape and size did not differ, but style was longer in tetraploids and seeds had a larger wing. Overall, these results supported a higher fitness in polyploids. Multivariate analysis showed continuous variation but consistent differentiation between diploid and tetraploid accessions. Taxonomically, the tetraploid populations at the eastern limit of the species range in the upper Tiber valley can be referred to a new subspecies, here described as O. bertolonii subsp. cesalpina.
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