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Understanding what makes a super food so resilient

The Carlsberg Foundation's 'Semper Ardens' Research Project

Quinoa was utilized as a food source by the Incas and is now recognized as probably the healthiest grain crop. Quinoa withstands extreme conditions of drought and salinity and therefore stands out as a crop already adapted to climate change. The mechanism by which quinoa is tolerant to salt stress is being investigated in this project.
By Michael Broberg Palmgren, DSc, PhD, Professor at Department of Plant and Environmental Sciences, University of Copenhagen

The Danish Nobel laureate prof. Jens Christian Skou discovered the sodium pump in crab nerves in 1957 and his student prof. Peter Leth Jørgensen helped us understand the mechanism by which this pump extrudes sodium ions from cells. 

In 1986, I carried out work for my master thesis in the laboratory of Peter Leth Jørgensen but ended up as a plant physiologist. However, ever since these early studies, it has remained a puzzle to me why plants do not have anything like this wonderful pump. 

Plants are very sensitive to sodium ions, which are not only toxic but also limit water uptake, and very few plants are able to grow in saline soils. Quinoa is one of these few plants that survives high salt. Elucidating its mechanism to cope with multiple water-related stresses would be key to breeding of crops with drought tolerance.

A Super nutritious Crop

An Ancient Super Crop

Quinoa originates from the South American Andes mountains where it seldom rains and salt deserts are widespread. Here it thrives at heights up to 4,000 meter above sea level in an extremely hostile environment which can be freezing cold (-4° to -8° C) during the night and unbearably hot (35° to 38° C) during the day. The Incas began cultivating this plant 3,000 to 4,000 years ago and it was their most popular crop together with potato.

Our body can produce only about half of the amino acids that we need to build up our proteins and the rest must come from the food we eat. Lysine is one such essential amino acid that we cannot produce ourselves and - unfortunately for vegetarians – many plant derived foods have little lysine but not quinoa. 

Quinoa seeds are rich in protein (the contents are 12-18%) and the amino acid composition of its proteins is close to the Food and Agriculture Organization (FAO) of the United Nations standard for humans and close to that of milk.

Quinoa seeds are also a source of linolenic acid (an omega-3 lipid) and linoleic acid (an omega-6 lipid), which are essential polyunsaturated fatty acids that we cannot produce ourselves, and the seeds also contain the natural antioxidant vitamin E that preserves these fragile lipids.  

Salt Tolerance of Quinoa

United Nations points to Quinoa

The Food and Agriculture Organization (FAO) of the United Nations has identified quinoa as the most nutritious per 100 calories of all grain crops and, to promote the use of quinoa worldwide, pronounced 2013 as The International Year of Quinoa.

Recently, quinoa has been studied as a model organism to investigate water-stress tolerance in plants. In 2017, high quality genome drafts were published based on inbred lines of two different quinoa cultivars. 

These genome sequences provide insight into the basis for the exceptional nutritional value of quinoa, and late in 2018, a bladder cell-specific transcriptome enabled the identification of candidate genes likely to be involved in salt tolerance. 

On this basis, we have proposed a model for how salt is dumped into bladder cells, which remains to be tested by mutagenesis of selected target genes.

Figure 1: A young leaf of quinoa with multiple bladder cells visible on its surface. Left, before brushing. Right, after gently brushing to remove the bladder cells. Photograph: Anton Frisgaard Nørrevang.

Our project partner Carlsberg Research Laboratory (CRL) recently devised a strategy to identify specific nucleotide substitutions in mutated genes. We are adapting Carlsberg’s mutation identification platform to achieve the following goals in quinoa: 

Epidermal bladder cells

Salt bladders on the outer skin of leaves (the epidermis) are cell structures homologous to epidermal hair cells. They are found in many salt-loving plants (halophytes), including quinoa, and have been proposed to be critical for their salt tolerance by serving as salt dumps. Ordinary hairs likely contribute to the drought tolerance of cereal grasses.

  1. Provide proof-of-concept that targeted chemical mutagenesis of quinoa is possible. 
  2. Mine the quinoa genome for natural variation in genes controlling drought and salt tolerance and transfer knowledge to other crops like barley and wheat. 
  3. Mutate targets in the quinoa genome that may facilitate agricultural use. 
  4. Mutate genes that are expressed in salt bladders and likely to be involved in water stress tolerance. 
  5. By phenotyping the mutated plants, test a previous hypothesis of water-stress tolerance in quinoa and generate new hypotheses.

Significance

Understanding the mechanisms of drought and salt tolerance in plants is a goal of exceptional fundamental interest and will have major practical applications by providing the basis for future breeding of water-stress resistant crops.

Figure 2: Bladder cells at higher magnifications. Photograph: Anton Frisgaard Nørrevang.

Developing non-GMO tools to screen for induced genetic variation in a specific quinoa gene will be a long-sought breakthrough that will benefit both basic research and agronomical breeding of this emerging climate-friendly crop.

Once the molecular identity of membrane transporters mediating salt loading into salt bladders, and the mechanisms regulating this process, are elucidated, this information could immediately be used by plant breeders. 

A first step would be beneficial to genetic variation in other Amaranthaceae crops (e.g. spinach, sugar beet and chard) or traditional crops (such as wheat or barley) and select for plant lines that express active sodium transporters in salt bladders and homologous epidermal hair cells, respectively, which may enable sodium sequestration outside metabolically active plant tissues. This addition to the plant breeding toolkit could deliver salt-tolerant crops to farmers’ fields.

Peer-Reviewed papers relevant to my research granted by the Carlsberg Foundation

  • López-Marqués RL, Nørrevang AF, Ache P, Moog M, Visintainer D, Wendt T, Østerberg JT, Dockter C, Jørgensen ME, Salvador AT, Hedrich R, Gao C, Jacobsen S-E, Shabala S, Palmgren M (2020) Prospects for accelerated improvement of the resilient crop quinoa. Journal of Experimental Botany (in press)
  • Y Zhang, M Pribil, M Palmgren, C Gao (2020) A CRISPR way for accelerating improvement of food crops. Nature Food 1: 200-205.
  • DeHaan L, Larson S, López-Marqués RL, Wenkel S, Gao C, Palmgren M (2020) Roadmap for accelerated domestication of an emerging perennial grain crop. Trends in Plant Science 25: 525-537.
  • Pedersen JT, Palmgren M (2017) Why do plants lack sodium pumps and would they benefit from having one? Functional Plant Biology 44: 473-479.

  • Østerberg JT, Xiang W, Olsen LI, Edenbrandt AK, Vedel SE, Christiansen A, Landes X, Andersen MM, Pagh P, Sandoe P, Nielsen J, Christensen SB, Thorsen BJ, Kappel K, Gamborg C, Palmgren M (2017) Accelerating the domestication of new crops: Feasibility and approaches. Trends in Plant Science 22: 373-384.

Other Relevant Papers in Scientific Journals and Newspapers as well as Relevant Media Communication

Fremtidens mad kan vandes med havvand - Kristeligt Dagblad

Quinoa er kernesund og kan modstå kommende klimaforandringer - Videnskab.dk

Danske forskere vil svække naturen for at skabe fremtidens mad - TV2 Lorry

Forskere vil udnytte fødevarepotentialet i 400.000 vilde plantearter - Sciencenews.dk