March 7, 2021
Agriculture futurist: Don Ort
Scientists have an ability to prove the predictions wrong, especially when it comes to meeting increasing food demand. In 1798, Thomas Malthus, an English political economist, published “An essay on the principle of population” in which he concluded that “The power of population is so superior to the power of the earth to produce subsistence for man, that premature death must in some shape or other visit the human race.” (Malthus, 1798). Over the centuries, this message has been repeated. For example, Paul Ehrlich’s 1968 book, The Population Bomb famously began with the statement “The battle to feed all of humanity is over. In the 1970s hundreds of millions of people will starve to death…” (Ehrlich, 1968). Through the expansion of cultivated land, intensification of inputs, and the adoption of resource-responsive dwarf varieties, the “Green Revolution” in the 60s and 70s, saw average annual production gains of 3.2% (1961–1980) across developing countries (80% of the gains due to yield ha−1 increases; e.g., Evenson and Gollin, 2003); forestalling a food crisis. Between 1981 and 2000, as world population grew by another 1.6 billion people, modern varieties and precision technologies continued to increase yield potential as well as reduce the yield gap between actual and potential yield. But analyses of production trends suggest the returns of the Green Revolution may be diminishing with yield gains stagnating (e.g., Ray et al., 2012). Thus, new approaches to meeting food demand will be required.
Meet Donald (Don) Ort—Robert Emerson Professor at University of Illinois—whose work is dedicated to increasing yield potential – the yield that can be attained under optimal management practices and in the absence of biotic and abiotic stresses – through improving photosynthetic efficiency. I ask him how he feels about being labeled an “agriculture futurist”: some of the solutions Don and his colleagues have proposed require redesigning photosynthesis and canopy light use; in other words, redesigning thousands of years of evolution. However, I consider him a futurist not because of this, but because his work predicts a point where we will be reliant on these ideas, and as such, the work of Don and his colleagues is already paving solutions to future crises. Accepting this proposition, I talk to him about how he got to this point and how increasing crop production has changed from one man—Norman Borlaug—using classic agronomic and Mendelian approaches, to a consortium effort utilizing physiological, computational, and synthetic biology approaches to come up with new ways to reimagine what is possible.
Our world is covered in plants and we depend on them, but how do they do what they do?
Don grew up on a few acres surrounded by plants, his summer job was in a nursery, and his backyard now boasts an apple orchard with 200 different genotypes, which he makes into cider, shares with colleagues, or with the Clydesdale horses up the road. Don’s love of growing plants has meant he has always gravitated to opportunities that have allowed him to cultivate his interests in plants and in particular answer the question of how plants work. After graduating from Wake Forest University, he was drawn to the plant research being undertaken at Michigan State University—“When I interviewed at Michigan State for my doctorate, there were faculty members who seemed to want to intimidate you. But then I walked into Norman Good’s lab and there was this guy in overalls scrubbing the floor. I asked him where Prof Good was, and he said he’ll be right back. The guy put down his mop, walked into Norman Good’s office, sat down at his desk and said I’m here now.” The contrast was enough for Don to know “this was someone I could work for.”
Shedding light on the fundamentals of photosynthesis
When Don entered the world of photosynthesis in 1971, engineering photosynthesis was not something he envisioned would be the goal of his research; nor a response to global climate change, which was not yet seen as a widespread challenge for agriculture (for reference, the Intergovernmental Panel on Climate Change was not formed until 1988). “We didn’t know what we know now.” However, from very early on, Don took a reductionist approach with the objective to “learn enough to start putting it back together”; a strategy which continues to guide Don’s thinking. Much of Don’s early work concentrated on understanding how the chemical and physical properties of the thylakoid membranes informed the mechanisms of energy transduction and ATP synthesis. His PhD, on “Studies on the mechanisms of conservation of redox energy and ATP by chloroplasts” was instrumental in proving that water oxidation itself produced two electrons and deposited two protons into the thylakoid lumen (Ort and Izawa, 1973). Later on, in his postdoctoral work in Richard (Dick) Dilley’s lab, he also provided experimental evidence in support of the idea that the pathway for proton transfer to drive ATP synthesis, could be localized along the membrane surface and not just via bulk flow between the lumen and stroma; as put forward by Mitchell in the chemiosmotic hypothesis (Mitchell, 1961). The two important observations from this work were that photophosphorylation could occur even in the presence of permeable buffers that abolish the pH difference between the lumen and stroma (Ort et al., 1976; Hangarter and Ort, 1985); and photophosphorylation could begin before proton distribution into the bulk phase occurred (Ort and Dilley, 1976; Ort et al., 1976). However, in the absence of a structure to support the observations and conflicting evidence, the debate of localized proton currents continues and remains an active question (e.g., Morelli et al., 2019), but for Don, one of the reasons he changed course was because he could not see where it was all going and whether that level of detail really mattered for furthering our understanding of photosynthesis.
Don was eager to ensure his efforts would have impact beyond the printed paper it was on. After a postdoctoral position at the University of Washington with William (Bill) Parson investigating proton transport using rhodopsin-containing purple bacteria in Halobacterium halobium (e.g., Ort and Parson, 1978), he made a conscious decision to pursue the mechanisms of environmental interactions in order to devise amelioration strategies for crop production. Accepting a position at the University of Illinois in 1978 (where he remains today), Don’s first question was “why is photosynthesis inhibited by cool but above-freezing temperatures in warm weather crops”—a liability that many of our cropping systems face. He demonstrated that photo-inhibition occurred under lower-temperature exposure in combination with even moderate irradiance levels (Martin and Ort, 1985), with evidence for direct damage to the photosynthetic apparatus by enhanced formation of oxygen radicals and damage to the oxidative side of PSII (Martin et al., 1981) and via inhibiting the repair of PSII (Grennan and Ort, 2007), as well as indirectly through a reduction in stromal bisphosphatases and subsequently CO2 assimilation, due to a lowered redox poise associated with the increase in oxidants (Sassenrath et al., 1987; Sassenrath et al., 1990; Hutchison et al., 2000). Through this work, it became obvious that despite enormous plasticity in the photosynthetic process, there were limits on the machinery to operate without impacting CO2 assimilation, raising alarm bells for Don of what this may mean in the context of rapid climate change.
We need to know what to expect as the climate changes
On sabbatical at Essex University in 1986, Don met Neil Baker and Stephen (Steve) Long (now Ikenberry University Chair of Plant Biology & Crop Sciences at the University of Illinois), where his interest in the impacts of climate change on crop production were cemented. Steve had already been working on the early Free-Air Carbon dioxide Enrichment (FACE) sites, and through a faculty of excellence program aimed at recruiting outstanding scientists, Don helped lure Steve to the University of Illinois in 1999 on the promise of helping to obtain funding for their own FACE site. In 2001, the establishment of “SoyFACE,” represented an important step in being able to quantify crop responses to elevated CO2 under field conditions. Significantly, they found the yield stimulation in C3 plants to be 50% less than that reported in enclosed experimental systems, warning of a large overestimation in future production estimates (Long et al., 2006). Further, as CO2 effects were investigated in combination with elevated temperature (e.g., Ruiz-Vera et al., 2013; Thomey et al., 2019), drought (e.g., Gray et al., 2016), and increased ozone concentrations (e.g., Morgan et al., 2004; Betzelberger et al., 2012), the interactions were almost always negative from the stand point of lowering the amount of stimulation associated with increased CO2. Thus, “it heighted the concern, that if we plant the same plants we are now, 10 or 20 years in the future, we are going to see very large drops in productivity.” This risk is real.
Based on increasing population growth and changes in food consumption patterns, food demand by 2050 is projected to double that of 2005 levels (Tilman et al., 2011). Stagnating annual yield increases in several major food crops (Ray et al., 2012) exacerbates the challenge, with the gap between average farm yield and genetic yield potential closing (Cassman, 1999) and the detrimental effects of climate change already being observed (Lobell and Field, 2007; Long and Ort, 2010). The next task had become obvious—“what can we do to acclimate plants [and increase yield potential]?” and two approaches were presented “go out and look for genetic variation in wild relatives and crop plants, and/or try to figure out mechanistically what’s going on, and then reengineer it.”
Scaling from the chloroplast to the canopy: solutions have tradeoffs
Yield potential (Yp) can be described as the total incident solar radiation across the growing season (St) multiplied by three genetically determined efficiency factors: how efficiently the light is intercepted (εi) and converted to biomass (εc), and then partitioned to the harvestable product (εp). Improvements in εi and εp were largely maximized in the Green Revolution (Hay, 1995; Sinclair, 1998), and thus hold little further potential for increasing the Yp. In comparison, a quantitative assessment of εc in crops grown in relatively nonstressed conditions indicated that realized εc is less than half the theoretical maxima (Slattery and Ort, 2015).
Advances in in silico crop modeling have been integral to understanding photosynthetic processes and their inefficiencies (Zhu et al., 2004; Zhu et al., 2008; Zhu et al., 2013) as well as predicting the outcomes of possible solutions (Ort et al., 2011; Song et al., 2017; Walker et al., 2018). The initial roadmap on how to improve photosynthetic efficiency in the near to long-term, was laid out in Zhu et al. (2010) and ended up being the lottery ticket to fund the ideas to fruition: “So it turns out, Bill Gates is very interested in photosynthesis and saw that table [outlining the timeline for the proposed solutions]”. Interested to learn more, the team was invited to pitch the ideas to the Bill and Melinda Gates Foundation, and from those discussions, the “Realising Increased Photosynthetic Efficiency” (RIPE) initiative was born! Since its inception in 2012, a number of proof-of-concepts have been achieved including the overexpression of key photosynthetic carbon reduction cycle enzymes in tobacco (Rosenthal et al., 2011) and soybean (Köhler et al., 2017); a photorespiratory bypass to reduce the amount of energy produced during photosynthesis that inevitably gets wasted through this pathway (South et al., 2019); and, reduced-chlorophyll mutants of soybean as a way to distribute light absorption more efficiently throughout the leaf layers (Slattery et al., 2017). All examples, have led to increased yields in field grown plants as a result of improved photosynthetic efficiency. These accomplishments have been acknowledged with a number of awards, not least, Don’s election to the National Academy of Sciences in 2017.
Of course, biology is full of complexity and therefore lessons—while some ideas were less challenging to implement than predicted (Long et al., 2018) others that were considered to be straight forward, remain elusive (e.g., introduction of cyanobacterial bicarbonate transporters into the chloroplast envelope; Rae et al., 2017) or likely to only show a biomass advantage under certain conditions (Głowacka et al., 2018). One important consideration is in the tradeoffs that occur when scaling from cellular to canopy level effects; which is exemplified in the case of reducing chlorophyll content described in the Founders Review by Slattery and Ort (2021). For example, light absorption may be greater at depth in a closed canopy, but early in the season before this occurs, reduced absorption results in increased light transmission to the soil (Slattery et al., 2017). Thus, the timing of chlorophyll reduction would need to be optimized for this strategy to reach its potential. It is perhaps because of these complexities that support for the idea of redesigning photosynthesis is not unanimous.
Reimagining photosynthesis takes courage and a multidisciplinary team
In 1999, Charles Mann—a science journalist for Science—wrote on the potential for agriculture to meet the 40% increase in food demand required by 2020. His piece was entitled “Crop scientists seek a new revolution” and in it he interviews a number of plant biologists about whether a bioengineering approach could be the answer. There’s a quote by crop physiologist, Thomas Sinclair (currently adjunct Professor at North Carolina State University), which I think is quite pertinent. He says: “If the question is whether farmers can raise average yields closer to the maximum, I would guess that there is [some room for improvement]. But if the question is whether breeders can raise the physiological potential of cereal crops … I don’t think the evidence there is very encouraging … it’s hard to see where improvement in that would come from.” (Mann, 1999). Sinclair echoes this sentiment in a recent piece (Sinclair et al., 2019). The challenge usually comes from the stand point that there is a reason evolution did not find a better solution. The response to this argument was given by Ort et al. (2015) in the description of the “smart canopy” whereby plants interact cooperatively to maximize the potential for light harvesting at the canopy level as opposed to the individual level where natural selection acts; an advancement on Donald’s weak competitive crop ideotype (Donald, 1968). Thus, it strikes me that redesigning photosynthesis takes vision and imagination.
Over the years, Ort and his colleagues have not been alone in the pursuit to boost photosynthesis—take James Bonner, a molecular biologist, who in 1962 wrote his thoughts on “The upper limit of crop yield” in Science: “might it not be possible to breed plants for such an improved and more sophisticated type of chloroplast structure? It seems today a difficult problem. Perhaps it is an insoluble one. But it is certainly a goal worthy of consideration. The fruits would be large indeed.” (Bonner, 1962). So, what has changed, especially given that the foundation for many of the ideas being pursued today were recognized in the early work of plant biologists; as acknowledged in the Founders Review (Slattery and Ort, 2021).
Firstly, we now have the computational power to model environmental dynamics, whereas previously we relied on (nonrealistic) steady-state processes, and already this increased capacity is delivering new solutions (Kromdijk et al., 2016; Taylor and Long, 2017); second, we have improved molecular tools to more efficiently transform gene targets; and, third, with the fortune of dedicated initiatives such as RIPE, pursuing parallel approaches has been possible, leading to research synergies and opportunities to foster early-career scientists; agriculture’s future. The next roadmap has been printed and in it a list of the tools that will need to be developed to support ongoing synthetic biology research into improving photosynthesis (Zhu et al., 2020); but, after talking with Don, these challenges seem achievable, and so I am excited by where the pursuit for knowledge and the scientific process will take us next. I certainly don’t think we will go hungry for ideas!