Calcium redistribution induces hard-to-cook phenotype and increases PHA-L lectin thermal stability in common bean low phytic acid 1 mutant seeds

Authors: COMINELLI, ELEONORA - Institute Of Biology And Agricultural Biotechnology; GALIMBERTI, MICHELA - Institute Of Biology And Agricultural Biotechnology; PONGRAC, PAULA - J Stefan Institute; LANDONI, MICHELA - University Of Milan; LOSA, ALESSIA - Institute Of Biology And Agricultural Biotechnology; PAOLO, DARIO - Institute Of Biology And Agricultural Biotechnology; DAMINATI, MARIA GLORIA - Institute Of Biology And Agricultural Biotechnology; BOLLINI, ROBERTO - Institute Of Biology And Agricultural Biotechnology; Cichy, Karen; VOGEL-MIKUS, KATARINA - J Stefan Institute; SPARVOLI, FRANCESCA - Institute Of Biology And Agricultural Biotechnology

Submitted to: Food Chemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/23/2020
Publication Date: 3/25/2020
Citation: Cominelli, E., Galimberti, M., Pongrac, P., Landoni, M., Losa, A., Paolo, D., Daminati, M., Bollini, R., Cichy, K.A., Vogel-Mikus, K., Sparvoli, F. 2020. Calcium redistribution induces hard-to-cook phenotype and increases PHA-L lectin thermal stability in common bean low phytic acid 1 mutant seeds. Food Chemistry. 32:126680. https://doi.org/10.1016/j.foodchem.2020.126680.
DOI: https://doi.org/10.1016/j.foodchem.2020.126680

Interpretive Summary: Phytic acid (PA) is the main compound used by seeds to store phosphorus for germinating seedlings. It also plays an important role in response to environmental stress and hormonal changes in plants. However, it is an antinutritional factor, because of its ability to chelate minerals important for human and animal nutrition into complexes that cannot be digested by monogastrics. To improve the nutritional quality of common beans, a biofortification program is underway focused on the reduction of PA content in seeds to increase the bioavailability of minerals. Low phytic acid (lpa) mutants in several crops, including common bean have been isolated and characterized. The lpa1 mutant common beans, exhibiting 90% reduction in seed PA concentration, has been shown to improve iron status in human trials, but adverse gastrointestinal effects have been reported and linked to the increased stability of a bean lectin, phytohemagglutinin L (PHA-L) in these seeds upon cooking. Moreover, it was suggested a hard to cook defect of the lpa1 seeds that seemed to intensify the problem. In the present work we confirmed the hard to cook phenotype of the lpa1 beans. We demonstrated that the lpa1 mutation strongly influences the stability of the PHA-L lectin but not that of the PHA-E lectin. We demonstrated that the mechanism by which the lpa1 mutation affects PHA-L stability involves an excess of free cations (most likely calcium, Ca2+) generated by the low levels of PA. We show that PHA-L thermal stability increases in presence of excess calcium during cooking and decreases in absence of divalent cations during cooking.

Technical Abstract: Chelation of minerals by phytic acid in seeds reduces mineral bioavailability. The consumption of common bean seeds with the low phytic acid 1 (lpa1) mutant improved iron status in human trials, but caused adverse gastrointestinal effects presumably due to the increased stability of lectin phytohemagglutinin L (PHA-L) in these seeds, compared to the wild type (wt) ones. A hard-to-cook (HTC) defect observed in the lpa1 seeds intensified the problem. We quantified the HTC phenotype of the lpa1 common beans in three genetic backgrounds. In one genetic background we correlated it to the redistribution of calcium, whose concentration in all parts of the seed and particularly in the cell walls was larger in the lpa1 compared to the wt, demonstrating the so-called “phytase-phytate-pectin” theory. Furthermore, the lpa1 mutation in combination with the presence of different PHA alleles affected the stability of the PHA-L lectin, due to an excess of free cations.