Ricinosomes and cell death in quinoa seeds

Quinoa (Chenopodium quinoa), a seed crop from the Andes region of South America, has been cultivated for the last 7000 years and is well adapted to extreme environmental conditions such as high altitude, low annual precipitation, high soil salinity and freezing temperatures. Quinoa is also valued as a crop because of its high nutritional value, particularly due to the exceptional amino acid balance of the seed protein and the quantity of nutritionally favourable lipids.

Quinoa seeds are disseminated with their pericarp covering the seed, constituting a characteristic utricular fruit. The pericarp is made up of papillose cells derived from the outer epidermis of the ovary wall and, below, tangentially stretched cellular remains. The seed coat consists of two cell layers: the exotesta and endotegmen. At maturity, cells of the pericarp and seed coat die. The three areas of food reserves in quinoa seeds are a large central perisperm, a peripheral embryo and an endosperm of one or two cell layers surrounding the radicle of the embryo. In the mature seed, the perisperm presents uniform, non-living, thin-walled cells, full of starch grains. Endosperm and embryo tissues, consisting of living cells, store proteins, lipids and minerals.

During the final stage of seed development, the cells of the lasting endosperm accumulate protein and lipids while the rest are crushed and disintegrated. Both the suspensor and endosperm die progressively from the innermost layers surrounding the embryo and extending towards the nucellar tissue. Ricinosomes are endoplasmic reticulum-derived organelles that accumulate both the pro-form and the mature form of cysteine endopeptidase, first identified in castor bean (Ricinus communis) endosperm during germination. This study sought to identify associations between the presence of ricinosomes and programmed cell death hallmarks in suspensor and endosperm cells predestined to die during quinoa seed development.

A recent paper in Annals of Botany describes a structural study of quinoa seed formation using light microscopy and transmission electron microscopy. Except for the one or two cell layers that constitute the lasting endosperm in the mature seed, ricinosomes were found in suspensor and endosperm cells. These cells were also the site of morphological abnormalities, including misshapen and fragmented nuclei, vesiculation of the cytosol, vacuole collapse and cell wall disorganization. This is the first report of the presence of these structures in the suspensor and endosperm of angiosperms during seed development. This result raises the possibility that the presence of ricinosomes or Cys-EP enzyme detection constitute an early hallmark that can be used to predict programmed cell death during development. Likewise, these observations regarding the structure and development of both the suspensor and endosperm are novel findings not only for the species but for the Amaranthaceae family in general.