Iron and ferritin accumulate in separate cellular locations in Phaseolus seeds

Abstract

BackgroundIron is an important micronutrient for all living organisms. Almost 25% of the world population is affected by iron deficiency, a leading cause of anemia. In plants, iron deficiency leads to chlorosis and reduced yield. Both animals and plants may suffer from iron deficiency when their diet or environment lacks bioavailable iron. A sustainable way to reduce iron malnutrition in humans is to develop staple crops with increased content of bioavailable iron. Knowledge of where and how iron accumulates in seeds of crop plants will increase the understanding of plant iron metabolism and will assist in the production of staples with increased bioavailable iron.ResultsHere we reveal the distribution of iron in seeds of three Phaseolus species including thirteen genotypes of P. vulgaris, P. coccineus, and P. lunatus. We showed that high concentrations of iron accumulate in cells surrounding the provascular tissue of P. vulgaris and P. coccineus seeds. Using the Perls' Prussian blue method, we were able to detect iron in the cytoplasm of epidermal cells, cells near the epidermis, and cells surrounding the provascular tissue. In contrast, the protein ferritin that has been suggested as the major iron storage protein in legumes was only detected in the amyloplasts of the seed embryo. Using the non-destructive micro-PIXE (Particle Induced X-ray Emission) technique we show that the tissue in the proximity of the provascular bundles holds up to 500 μg g-1 of iron, depending on the genotype. In contrast to P. vulgaris and P. coccineus, we did not observe iron accumulation in the cells surrounding the provascular tissues of P. lunatus cotyledons. A novel iron-rich genotype, NUA35, with a high concentration of iron both in the seed coat and cotyledons was bred from a cross between an Andean and a Mesoamerican genotype.ConclusionsThe presented results emphasize the importance of complementing research in model organisms with analysis in crop plants and they suggest that iron distribution criteria should be integrated into selection strategies for bean biofortification.

Genetic control of iron concentration in Mesoamerican and Andean common bean seeds

“…Therefore, the highest accumulation of iron was found in the seed coats of Mesoamerican common bean seeds, which agrees with the results of Ariza-Nieto et al (2007), Cvitanich et al (2010), and Ribeiro et al (2012). The iron present in the seed coat of the common bean seeds was more bioavailable to the human body (Lombardi-Boccia et al, 1995).…”

“…The distribution of iron between the embryo and the seed coat fractions of common bean seeds can vary among gene pools, as observed in the present study and by Ariza-Nieto et al (2007), Cvitanich et al (2010), Ribeiro et al (2012), and Blair et al (2013). Since iron is accumulated more in the embryo of the Andean Pesq.…”

“…Therefore, in the Andean gene pool, the seeds of the F 1 generation represented the product of the fertilization between the parents, because most of the iron (69.40 to 73.44%) was concentrated in the embryo of the seeds (Table 2). Ariza-Nieto et al (2007) and Cvitanich et al (2010) also described Cal 96 as a major iron accumulator line in the seed embryo. In this case, the selection for increased iron concentration in the Andean common bean should be done on the F 2 generation seeds, when maximum genetic variability can be accessed.…”

“…agropec. bras., Brasília, v.50, n.5, p.383-391, maio 2015 DOI: 10.1590/S0100-204X2015000500005 However, the distribution of iron in the embryo and seed coat fractions of common bean seeds varies among gene pools and between lines of the same gene pool (Moraghan et al, 2002;Ariza-Nieto et al, 2007;Cvitanich et al, 2010;Ribeiro et al, 2012;Blair et al, 2013). This has direct consequences on iron bioavailability for the human organism (Lombardi-Boccia et al, 1995), in deciding when to start the process of selection of superior lines (Jost et al, 2009) and to determine the initial vigor of common bean seeds (Moraghan et al, 2002).…”

Nutritionally Enhanced Staple Food Crops

“…Common bean and soybean genotypes were reported to accumulate different proportion of total seed Fe in the seed coat, embryo, and cotyledons (Laszlo 1990;Moraghan 2004;Ariza-Nieto et al 2007;Cvitanich et al 2010Cvitanich et al , 2011, indicating that specific tissues relevant for Fe storage should be identified and their Fe loading mechanisms be investigated to exploit such variability toward developing seed iron-dense cultivars. Using (-PIXE assay to investigate Fe distribution in seed tissues of Phaseolus species, Cvitanich et al (2010Cvitanich et al ( , 2011 concluded that (1) the distribution of Fe in seed depends on the species and genotype, (2) high concentrations of Fe accumulate in cells surrounding the provascular tissue, (3) the tissue in the proximity of the provascular bundles holds up to 500 mg g À1 Fe, depending on genotypes, and (4) the largest proportion of seed Fe in Phaseolus species is stored in compounds and cell parts different from ferritin and starch vacuoles. These results indicate that more studies are needed to assess the patterns of micronutrient distribution in seeds, and that micronutrient distribution criteria should be integrated into the selection strategies for biofortification of staple crops.…”