Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation

Filatov, Victor; Dowdle, John; Smirnoff, Nicholas; Ford‐Lloyd, B. V.; Newbury, H. J.; Macnair, Mark R.

doi:10.1111/j.1365-294x.2006.02981.x

Cited by 73 publications

(99 citation statements)

References 33 publications

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“…In A. halleri and T. caerulescens, NRAMP3 is highly expressed in roots. AhNRAMP3 is also highly expressed in shoots, whereas NRAMP1 and NRAMP5 are highly expressed in shoots of T. caerulescens [44,[46][47][48][49]. The primary biological function of A. thaliana NRAMP transporters appears to be in Fe homeostasis.…”

Section: Nramp Transportersmentioning

confidence: 99%

Transition metal transport

2007

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Transition metal transporters are of central importance in the plant metal homeostasis network which maintains internal metal concentrations within physiological limits. An overview is given of the functions of known transition metal transporters in the context of the unique chemical properties of their substrates. The modifications of the metal homeostasis network associated with the adaptation to an extreme metalliferous environment are illustrated in two Brassicaceae metal hyperaccumulator model plants based on cross-species transcriptomics studies. In a comparison between higher plants and unicellular algae, hypotheses are generated for evolutionary changes in metal transporter complements associated with the transition to multicellularity.

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Section: Nramp Transportersmentioning

confidence: 99%

Transition metal transport

2007

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“…Zn tolerance and Zn accumulation remain unlinked in A. halleri: Recently, an interspecific crossing scheme between A. halleri and A. l. petraea was used for identifying QTL involved in Zn accumulation in A. halleri (Filatov et al 2006). By comparing gene expression of Zn-accumulating F 3 families to non-Zn-accumulating F 3 families, the authors identified 237 genes that were more expressed in the accumulating progenies.…”

Section: Previous Combinations Of Classical Functional and Transcriptmentioning

confidence: 99%

“…By comparing gene expression of Zn-accumulating F 3 families to non-Zn-accumulating F 3 families, the authors identified 237 genes that were more expressed in the accumulating progenies. Deducing the chromosomal position of these genes from the A. l. petraea linkage map reported by Kuittinen et al (2004), the authors identified 20 and 18 adjacent genes, respectively, belonging to two regions located on chromosomes 3 and 7 (Filatov et al 2006), corresponding to LG3 and LG7 of the Ah 3 Alp map. None of these regions were identified in the QTL analysis of Zn tolerance reported here.…”

Section: Previous Combinations Of Classical Functional and Transcriptmentioning

confidence: 99%

“…We performed an interspecific cross between A. halleri from a highly contaminated industrial site and A. l. petraea to generate a first-generation backcross (BC 1 ). These progeny, segregating for Zn tolerance, were used to construct a molecular linkage map (the first reported for a cross between these two species) and to identify QTL regions for Zn tolerance in A. halleri, making full use of the previous mapping experiments conducted on A. lyrata subspecies (Kuittinen et al 2004;Yogeeswaran et al 2005) and of recent and current functional analyses of metal homeostasis genes in A. halleri (Becher et al 2004;Weber et al 2004;Filatov et al 2006).…”

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confidence: 99%

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The Genetic Basis of Zinc Tolerance in the Metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): An Analysis of Quantitative Trait Loci

et al. 2007

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The species Arabidopsis halleri, an emerging model for the study of heavy metal tolerance and accumulation in plants, has evolved a high level of constitutive zinc tolerance. Mapping of quantitative trait loci (QTL) was used to investigate the genetic architecture of zinc tolerance in this species. A firstgeneration backcross progeny of A. halleri ssp. halleri from a highly contaminated industrial site and its nontolerant relative A. lyrata ssp. petraea was produced and used for QTL mapping of zinc tolerance. A genetic map covering most of the A. halleri genome was constructed using 85 markers. Among these markers, 65 were anchored in A. thaliana and revealed high synteny with other Arabidopsis genomes. Three QTL of comparable magnitude on three different linkage groups were identified. At all QTL positions zinc tolerance was enhanced by A. halleri alleles, indicating directional selection for higher zinc tolerance in this species. The two-LOD support intervals associated with these QTL cover 24, 4, and 13 cM. The importance of each of these three regions is emphasized by their colocalization with HMA4, MTP1-A, and MTP1-B, respectively, three genes well known to be involved in metal homeostasis and tolerance in plants.M ETAL tolerance in plants has been considered ''an example of more powerful evolution in action than industrial melanism in moths' ' (Antonovics et al. 1971). Therefore it has been the focus of many evolutionary studies, in which it was argued that metal tolerance could evolve rapidly following exposure to heavy metal stress (Wu et al. 1975;Al-Hiyali et al. 1988). Some heavy metals, like zinc and copper, are oligo-nutrients and thus essential in small quantities for normal plant development. To avoid metal toxicity, all plants have evolved basic tolerance mechanisms. Binding by proteins or nonprotein thiol peptides in the cytoplasm and subsequent sequestration in the vacuole are the major component processes in the cellular heavy metal detoxification (Clemens 2001;Krämer 2005). However, at so-called metalliferous sites, heavy metals can occur at highly elevated concentrations in the soil, either through ancient natural processes, as in nickel-rich serpentine soils, or through recent human activities, as in zinc-and cadmium-rich calamine soils surrounding smelters. The total metal content of contaminated sites, depending on the metal, can be up to 10-to 1000-fold higher than that of uncontaminated sites (Bert et al. 2002). At these extreme concentrations, both essential and nonessential heavy metals become toxic (Clemens 2001;Hall 2002) and only a small number of plant species have evolved tolerance to such concentrations. These species have been classified as either absolute (strict or eu-) or facultative (pseudo-) metallophytes, according to their occurrence either on contaminated sites only or on both metalliferous and nonmetalliferous soils (Lambinon and Auquier 1964).The genetic basis of adaptive quantitative traits is still the matter of strong debates among evolutionists. Current que...

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“…Among those metal-tolerant plants, some possess a remarkable physiological trait called hyperaccumulation that enables them to tolerate and accumulate high heavy metal concentrations in their shoots (about 100 times those occurring in nonaccumulator plants growing in the same substrates). Metal hyperaccumulators are consequently a particularly valuable resource to study the genetic basis of metal homeostasis.Arabidopsis halleri is an emerging model species for the molecular elucidation of metal tolerance and hyperaccumulation (Becher et al, 2004;Weber et al, 2004;Craciun et al, 2006;Filatov et al, 2006). This species belongs to the family Brassicaceae and shares about 94% DNA sequence identity within coding regions with the non-metal-tolerant plant species Arabidopsis (Arabidopsis thaliana; Becher et al, 2004).…”

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A Major Quantitative Trait Locus for Cadmium Tolerance in Arabidopsis halleri Colocalizes with HMA4, a Gene Encoding a Heavy Metal ATPase

Courbot¹,

Willems²,

Motté³

et al. 2007

Plant Physiol.

281

228

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Cadmium (Cd) tolerance seems to be a constitutive species-level trait in Arabidopsis halleri sp. halleri. Therefore, an interspecific cross was made between A. halleri and its closest nontolerant interfertile relative, Arabidopsis lyrata sp. petraea, and a firstgeneration backcross population (BC1) was used to map quantitative trait loci (QTL) for Cd tolerance. Three QTL were identified, which explained 43%, 24%, and 16% of the phenotypic variation in the mapping population. Heavy metal transporting ATPases4 (HMA4), encoding a predicted heavy metal ATPase, colocalized with the peak of the major QTL Cdtol-1 and was consequently further studied. HMA4 transcripts levels were higher in the roots and the shoots of A. halleri than in A. lyrata sp. petraea. Pollutants such as heavy metals can occur at very high concentrations in the soil as a consequence of either ancient natural processes or recent human activities such as mining, industrial, and agricultural practices. Although heavy metals are very toxic at high concentrations, some metal-tolerant plant species have developed the ability to grow and reproduce on soils highly polluted by heavy metals (Macnair, 1987). Among those metal-tolerant plants, some possess a remarkable physiological trait called hyperaccumulation that enables them to tolerate and accumulate high heavy metal concentrations in their shoots (about 100 times those occurring in nonaccumulator plants growing in the same substrates). Metal hyperaccumulators are consequently a particularly valuable resource to study the genetic basis of metal homeostasis.Arabidopsis halleri is an emerging model species for the molecular elucidation of metal tolerance and hyperaccumulation (Becher et al., 2004;Weber et al., 2004;Craciun et al., 2006;Filatov et al., 2006). This species belongs to the family Brassicaceae and shares about 94% DNA sequence identity within coding regions with the non-metal-tolerant plant species Arabidopsis (Arabidopsis thaliana; Becher et al., 2004). A. halleri constitutively tolerates zinc (Zn;Pauwels et al., 2006) and so far all the identified accessions are able to tolerate cadmium (Cd) and to hyperaccumulate Zn (Macnair et al., 1999). Hyperaccumulation of Cd was

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Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation

Cited by 73 publications

References 33 publications

Transition metal transport

Transition metal transport

The Genetic Basis of Zinc Tolerance in the Metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): An Analysis of Quantitative Trait Loci

A Major Quantitative Trait Locus for Cadmium Tolerance in Arabidopsis halleri Colocalizes with HMA4, a Gene Encoding a Heavy Metal ATPase

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