Contents Summary 677 Physical and chemical properties of zinc 678 Biochemical properties of zinc 678 Proteins interacting with zinc 678 Zinc fluxes in the soil–root–shoot continuum 679 Zinc in plants 684 Plant responses to elevated soil Zn 686 Acknowledgements 695 References 696 Summary Zinc (Zn) is an essential component of thousands of proteins in plants, although it is toxic in excess. In this review, the dominant fluxes of Zn in the soil–root–shoot continuum are described, including Zn inputs to soils, the plant availability of soluble Zn2+ at the root surface, and plant uptake and accumulation of Zn. Knowledge of these fluxes can inform agronomic and genetic strategies to address the widespread problem of Zn‐limited crop growth. Substantial within‐species genetic variation in Zn composition is being used to alleviate human dietary Zn deficiencies through biofortification. Intriguingly, a meta‐analysis of data from an extensive literature survey indicates that a small proportion of the genetic variation in shoot Zn concentration can be attributed to evolutionary processes whose effects manifest above the family level. Remarkable insights into the evolutionary potential of plants to respond to elevated soil Zn have recently been made through detailed anatomical, physiological, chemical, genetic and molecular characterizations of the brassicaceous Zn hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri.
Plants constantly sense the changes in their environment; when mineral elements are scarce, they often allocate a greater proportion of their biomass to the root system. This acclimatory response is a consequence of metabolic changes in the shoot and an adjustment of carbohydrate transport to the root. It has long been known that deficiencies of essential macronutrients (nitrogen, phosphorus, potassium and magnesium) result in an accumulation of carbohydrates in leaves and roots, and modify the shoot-to-root biomass ratio. Here, we present an update on the effects of mineral deficiencies on the expression of genes involved in primary metabolism in the shoot, the evidence for increased carbohydrate concentrations and altered biomass allocation between shoot and root, and the consequences of these changes on the growth and morphology of the plant root system. Responses of plants to mineral deficienciesPlant growth and development ultimately depend upon environmental variables, such as temperature, light intensity and the availability of water and essential minerals. One of the mechanisms by which plants adjust to an imbalance of exogenous resources is by allocating new biomass to the organs that are involved in acquiring the resources that are scarcest [1]. Studies examining the relationships between mineral nutrition and plant growth and development have been undertaken, but most work has focussed on elucidating ion transport mechanisms and the biochemical pathways affected by mineral deficiencies [2][3][4]. Many reviews provide a comprehensive picture of the nature of mineral acquisition from the soil, transport within the plant and homeostasis in the plant cell [5][6][7][8][9][10]. However, progress is slow in understanding the molecular and physiological events responsible for sensing and signalling mineral resource limitation and their ultimate effects on plant development and biomass allocation. Now, with the emergence of microarray technologies to monitor gene expression, plant physiologists have begun to investigate the rapid transcriptional changes associated with mineral imbalance [11][12][13][14][15][16][17][18][19][20][21][22][23]. There is also considerable interest in the functional connection between the genome and the complement of ions in the cell (the ionome) [24].Deficiencies of nitrogen (N) [20,[25][26][27][28][29][30][31] and phosphorus (P) [7,[32][33][34][35][36][37] result in accumulation of carbohydrate in leaves, higher levels of carbon allocated to the root and an increase in root-to-shoot (R:S) biomass ratio. N and P deficiencies therefore affect, to various extents, primary photosynthesis, sugar metabolism and/or carbohydrate partitioning between source and sink tissues. By contrast, although leaves of potassium (K)-deficient [32,33,38,39] and magnesium (Mg)-deficient [32,33,[40][41][42][43] plants accumulate sugars, they rarely increase their root biomass. This is likely to be a consequence of impaired sucrose export from leaves of K-and Mg-deficient plants, rather than a change in p...
(J.P.H., M.J.B., S.T.M., R.S.)Our aim was to generate and prove the concept of "smart" plants to monitor plant phosphorus (P) status in Arabidopsis. Smart plants can be genetically engineered by transformation with a construct containing the promoter of a gene upregulated specifically by P starvation in an accessible tissue upstream of a marker gene such as -glucuronidase (GUS). First, using microarrays, we identified genes whose expression changed more than 2.5-fold in shoots of plants growing hydroponically when P, but not N or K, was withheld from the nutrient solution. The transient changes in gene expression occurring immediately (4 h) after P withdrawal were highly variable, and many nonspecific, shock-induced genes were up-regulated during this period. However, two common putative cis-regulatory elements (a PHO-like element and a TATA box-like element) were present significantly more often in the promoters of genes whose expression increased 4 h after the withdrawal of P compared with their general occurrence in the promoters of all genes represented on the microarray. Surprisingly, the expression of only four genes differed between shoots of P-starved and -replete plants 28 h after P was withdrawn. This lull in differential gene expression preceded the differential expression of a new group of 61 genes 100 h after withdrawing P. A literature survey indicated that the expression of many of these "late" genes responded specifically to P starvation. Shoots had reduced P after 100 h, but growth was unaffected. The expression of SQD1, a gene involved in the synthesis of sulfolipids, responded specifically to P starvation and was increased 100 h after withdrawing P. Leaves of Arabidopsis bearing a SQD1::GUS construct showed increased GUS activity after P withdrawal, which was detectable before P starvation limited growth. Hence, smart plants can monitor plant P status. Transferring this technology to crops would allow precision management of P fertilization, thereby maintaining yields while reducing costs, conserving natural resources, and preventing pollution.
Sugars in plants, derived from photosynthesis, act as substrates for energy metabolism and the biosynthesis of complex carbohydrates, providing sink tissues with the necessary resources to grow and to develop. In addition, sugars can act as secondary messengers, with the ability to regulate plant growth and development in response to biotic and abiotic stresses. Sugar-signalling networks have the ability to regulate directly the expression of genes and to interact with other signalling pathways. Photosynthate is primarily transported to sink tissues as sucrose via the phloem. Under phosphorus (P) starvation, plants accumulate sugars and starch in their leaves. Increased loading of sucrose to the phloem under P starvation not only functions to relocate carbon resources to the roots, which increases their size relative to the shoot, but also has the potential to initiate sugar-signalling cascades that alter the expression of genes involved in optimizing root biochemistry to acquire soil phosphorus through increased expression and activity of inorganic phosphate transporters, the secretion of acid phosphatases and organic acids to release P from the soil, and the optimization of internal P use. This review looks at the evidence for the involvement of phloem sucrose in co-ordinating plant responses to P starvation at both the transcriptional and physiological levels.
The environmental and financial costs of using inorganic phosphate fertilizers to maintain crop yield and quality are high. Breeding crops that acquire and use phosphorus (P) more efficiently could reduce these costs. The variation in shoot P concentration (shoot-P) and various measures of P use efficiency (PUE) were quantified among 355 Brassica oleracea L. accessions, 74 current commercial cultivars, and 90 doubled haploid (DH) mapping lines from a reference genetic mapping population. Accessions were grown at two or more external P concentrations in glasshouse experiments; commercial and DH accessions were also grown in replicated field experiments. Within the substantial species-wide diversity observed for shoot-P and various measures of PUE in B. oleracea, current commercial cultivars have greater PUE than would be expected by chance. This may be a consequence of breeding for increased yield, which is a significant component of most measures of PUE, or early establishment. Root development and architecture correlate with PUE; in particular, lateral root number, length, and growth rate. Significant quantitative trait loci associated with shoot-P and PUE occur on chromosomes C3 and C7. These data provide information to initiate breeding programmes to improve PUE in B. oleracea.
The calcium (Ca) concentration of plant shoot tissues varies systematically between angiosperm orders. The phylogenetic variation in the shoot concentration of other mineral nutrients has not yet been described at an ordinal level. The aims of this study were (1) to quantify the shoot mineral concentration of different angiosperm orders, (2) to partition the phylogenetic variation in shoot mineral concentration between and within orders, (3) to determine if the shoot concentration of different minerals are correlated across angiosperm species, and (4) to compare experimental data with published ecological survey data on 81 species sampled from their natural habitats. Species, selected pro rata from different angiosperm orders, were grown in a hydroponic system under a constant external nutrient regime. Shoots of 117 species were sampled during vegetative growth. Significant variation in shoot carbon (C), calcium (Ca), potassium (K), and magnesium (Mg) concentration occurred between angiosperm orders. There was no evidence for systematic differences in shoot phosphorus (P) or organic-nitrogen (N) concentration between orders. At a species level, there were strong positive correlations between shoot Ca and Mg concentration, between shoot P and organic-N concentration, and between shoot K concentration and shoot fresh weight:dry weight ratio. Shoot C and cation concentration correlated negatively at a species level. Species within the Poales and the Caryophyllales had distinct shoot mineralogies in both the designed experiment and in the ecological survey.
The use of micro-array technology has allowed researchers to catalogue the genetic responses of plants to P deficiency. Genes whose expression is altered by P deficiency include various transcription factors, which are thought to coordinate plant responses to P deficiency, and other genes involved in P acquisition and tissue P economy. Several common cis-regulatory elements have been identified in the promoters of these genes, suggesting that their expression might be coordinated. It is suggested that knowledge of the genes whose expression changes in response to P deficiency might allow the development of crops with improved PUE, and could be used in diagnostic techniques to monitor P deficiency in crops either directly using 'smart' indicator plants or indirectly through transcript profiling. The development of crops with improved PUE and the adoption of diagnostic technology could reduce production costs, minimize the use of a non-renewable resource, reduce pollution and enhance biodiversity.
Summary• Whole-genome transcriptome profiling is revealing how biological systems are regulated at the transcriptional level. This study reports the development of a robust method to profile and compare the transcriptomes of two nonmodel plant species, Thlaspi caerulescens , a zinc (Zn) hyperaccumulator, and Thlaspi arvense , a nonhyperaccumulator, using Affymetrix Arabidopsis thaliana ATH1-121501 GeneChip® arrays (Affymetrix, Santa Clara, CA, USA).• Transcript abundance was quantified in the shoots of agar-and compost-grown plants of both species. Analyses were optimized using a genomic DNA (gDNA)-based probe-selection strategy based on the hybridization efficiency of Thlaspi gDNA with corresponding A. thaliana probes. In silico alignments of GeneChip® probes with Thlaspi gene sequences, and quantitative real-time PCR, confirmed the validity of this approach.• Approximately 5000 genes were differentially expressed in the shoots of T. caerulescens compared with T. arvense , including genes involved in Zn transport and compartmentalization.• Future functional analyses of genes identified as differentially expressed in the shoots of these closely related species will improve our understanding of the molecular mechanisms of Zn hyperaccumulation.
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