Selenium accumulation, distribution and speciation in spineless prickly pear cactus: a salt, boron, and drought tolerant, selenium-enriched nutraceutical fruit crop.

Authors: Banuelos, Gary; FAKRA, SIRINE - The Institute For Advanced Learning And Research; Walse, Spencer; MARCUS, MATTHEW - The Institute For Advanced Learning And Research; YANG, SOO IN - University Of California; PICKERING, INGRID - University Of California; PILON-SMITS, ELIZABETH - Colorado State University; FREEMAN, JOHN - Fresno State University

Submitted to: Journal of Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/15/2010
Publication Date: 1/1/2011
Citation: Banuelos, G.S., Fakra, S.C., Walse, S.S., Marcus, M.A., Yang, S., Pickering, I.J., Pilon-Smits, E.A., Freeman, J.L. 2011. Selenium accumulation, distribution and speciation in spineless prickly pear cactus: a salt, boron, and drought tolerant, selenium-enriched nutraceutical fruit crop. Journal of Plant Physiology. 155:315-327.

Interpretive Summary: The increased accumulation of naturally-occurring salts, Se and boron (B) has worsened in some agricultural areas, e.g., westside of central California, due to limited fresh water supplies, low winter rainfall and drought conditions, which reduces leaching away from the root zone. Consequently, for irrigated agriculture to survive and be sustained in such arid regions, it is crucial to identify alternative crops that are drought, salt and B tolerant. Since Se is also an essential micronutrient, an emerging concept to utilize such areas is to grow potential Se biofortified crops. Prickly pear cactus, Opuntia, is an attractive crop in this application because the dark purple fruit have medicinal benefits and some varieties tolerate drought, salt and B while accumulating and volatilizing Se. Without Se enrichment, Opuntia fruit and cladode already contain chemotherapeutic qualities that when eaten have been shown to help protect the human immune and nervous systems, prevent oxidative stress, help treat; gastritis, hyperglycemia, arteriosclerosis, diabetes, prostatic hypertrophy, and to help prevent multiple human cancers. There appears to be a clear potential for producing value added Se enriched Opuntia as a low maintenance drought tolerant crop with nutritional and health benefits. These features are consistent with production when grown in the drought, salt, B and Se impacted agricultural areas such as those located on the West side of central California. However, the biochemistry and speciation of Se in Opuntia, or in any cactus species, is unknown. Based on earlier field measurements we hypothesized that the spineless prickly pear cactus Opuntia ficus-indica (L.) Mill. may have a Se metabolism comparable to secondary Se accumulator plant species. Hence, the objectives of this study were to quantify accumulation, spatial distribution and chemical speciation of Se in the organs of spineless, salt tolerant, antioxidant rich, dark purple fruit bearing, Opuntia. We achieved this by using a combination of synchrotron X-ray absorption spectroscopy and mass spectrometry techniques to identify the selenium compounds within Se-enriched Opuntia tissue. The investigation of the biochemistry and molecular biology of selenium in Opuntia tissue has yielded insights into the physiology of selenium in this cactus and may have global agronomic applications that can improve human health and remediate Se polluted environments. We conclude that because of the two Se forms (selenocystathionine and selenomethionine) present, Opuntia may have a strong application as a Se enriched nutraceutical dietary source with potential for improving human mineral nutrition, while possibly preventing cancer, heart disease, virus and bacterial infections.

Technical Abstract: Prickly pear cactus (Opuntia) may be an alternative crop to grow in drainage-impacted regions of the westside of California, where high levels of salinity, selenium (Se), and boron (B) are present. Preliminary trials have demonstrated that Opuntia can tolerate the adverse soil conditions, while accumulating Se. Producing Se-enriched plant products may be of high nutritional value, depending on the form of Se found within the plant. The organ specific accumulation, spatial distribution and chemical speciation of selenium (Se) is not known for any cactus species. This was investigated in Opuntia ficus-indica (L.) Mill. using inductively coupled plasma mass spectrometry (ICPMS), micro-focused X-ray fluorescence elemental and chemical mapping (µXRF), X-ray absorption near edge structure (XANES) and liquid chromatography mass spectrometry (LCMS). Micro-XRF showed Se concentrated in young cladode conic-vestigial leaves (tips), the cladode vasculature and in the seed embryo. XANES demonstrated that 94% of total Se in cladode, fruit juice, fruit pulp and seed were C-Se-C compounds. Cladode tips contained 42% selenate and 58% C-Se-C forms. ICPMS quantification of Se in HPLC fractions followed by LCMS analysis showed the C-Se-C compounds in mature organs to be selenocystathionine (SeCyst) and selenomethionine (SeMet) in a SeCyst:SeMet ratio of 75:25 cladode, 71:29 fruit, and 32:68 seed. Enzymatic digestions and subsequent analysis confirmed that Se was mainly found in a “free” non-proteinaceous form in cladode and fruit, and was mostly in proteins associated with lipids in the seed. Micro-XRF chemical mapping illuminated the transition from selenate in the cladode tips into the two identified C-Se-C forms primarily accumulated in the cladode mesophyll. We conclude that Opuntia is a secondary Se accumulating plant whose fruit and cladode accumulate mostly SeCyst and some SeMet, while seeds contain mainly SeMet. When eaten the organic Se forms in Opuntia fruit, cladode and seed may improve health, increase Se mineral nutrition and help prevent multiple human cancers.