What Is the Next Frontier in Plant Engineering?

Urgency and Opportunity

Jeff Dangl

HHMI and University of North Carolina at Chapel Hill, North Carolina

Population growth, climate change, and changes in water availability will alter the face of civilization over the next 50 years. Consequent effects on food production systems necessitate that we increase crop yields by 30%–50% to meet the demands of growing populations. Most pressure will fall on populations already at the margins for food production and water sustainability. Developed countries will also suffer as water resources are depleted at rates that exceed recharge from rainfall, as extreme drought becomes commonplace, and as plant pests and pathogens inhabit new host ranges as a consequence of climate change.

There has never been more urgency for a deeper understanding of basic plant biology and for acceleration of crop development. Genome editing tools have yielded novel developmental features like higher tomato fruit yield, healthier oils, and resistance to powdery mildew disease. Definition and dissection of plant-associated microbiomes promise development of probiotics to enhance plant performance. Deep knowledge of plant development, the plant immune system, and plant metabolism—based on continued exploitation of models like Arabidopsis and rice—can now be extended to any crop species. It’s an exciting time for plant biology, basic and applied, and the importance of plant science has never been greater.

Mining Metabolites

Anne Osbourn

John Innes Centre, Norwich, UK

Plants produce a wealth of drugs and other useful natural products. Many of these compounds are structurally complex and beyond the reach of chemical synthesis. Availability is limited by difficulties in accessing source species, low yield, purification problems, and environmental concerns. The scale of the economic opportunity for improving the supply of high-value products from plants is therefore enormous. Of the >1 million metabolites estimated to be produced by plants, the genes are only known for ~50 complete pathways. Thus, current understanding of plant metabolic diversity is scant and highly fragmented. However, technical advances and reduced costs are accelerating sequencing of plant genomes with plans underway to sequence tens of thousands. This vast new resource, in combination with advances in computational and synthetic biology, will make it feasible to map out the “dark matter” of plant genomes that determines metabolic diversity, with the ultimate aim of harnessing and expanding on the full chemical engineering capability of the plant kingdom. By developing a translational synthetic biology pipeline for rapid preparative access to plant natural products and novel analogs, it should ultimately be possible to make designer molecules for specific applications on demand.

Synthetic Signaling Circuits

Diego Orzáez

IBMCP-CSIC, Valencia, Spain

Plant physiological outputs with strong impact in agriculture, such as developmental phase transitions or stress responses, are tightly controlled by intricate regulatory networks for which our intervention capacity is currently very limited. An exciting bioengineering challenge will consist of equipping plants with synthetic signaling circuits that interact with those networks. Synthetic circuits would enable us to take control of relevant natural processes such as flowering time, temperature, and drought responses or to switch newly engineered programs like synthetic defense mechanisms or added-value metabolic pathways, thus avoiding the deleterious effects of constitutive activation. Progressing in this direction will require engineering new sensors whose inputs can be deployed safely in the field—namely protein- or RNA-based receptors sensing environmentally friendly agrochemicals or optogenetic inputs. Signals will need to be transduced by orthogonal genetic processors and deployed to genetic actuators, likely programmable transcriptional regulators based on CRISPR/Cas9 architecture, which connect to endogenous factors to produce the desired output. The recent experience in rewiring microbial systems suggests that a synthetic biology approach based on the design of exchangeable modular elements that undergo iterative design-build-test cycles using easily screenable biological systems is the most effective direction to take in this new frontier of green bioengineering.

Breeding by Design

Zhikang Li

Chinese Academy of Agricultural Sciences, China

Many plant scientists are optimistic that “plant engineering” may provide solutions to the challenge of developing highly productive and environment-resilient crop cultivars for future food security. Historically, successes in plant improvement have been built primarily upon the utilization of the genetic diversity of germ-plasms, but conventional breeding based on line crossing and phenotypic selection is inefficient and based largely on experience. With the advent of DNA-sequencing technologies, reference genomes of most crops and economic plants are available. The genomic variation of the core collections of germplasms are being revealed for major crops by resequencing. Tremendous efforts have been taken to link the genomic variation (SNPs, haplotypes, gene presence/absence variations, and cryptic structural variations) with phenotypes. These advances, together with the global progress in plant functional genomics, are opening a new era of plant engineering: breeding by design. However, the greatest challenge is how to use the “incomplete” information at large numbers of loci for improving multiple complex traits in a highly efficient way. Fortunately, strong phenotypic selection for abiotic stress tolerances in segregating plant populations may often cause “genome shocks” characterized by genome-wide loss of heterozygosity or alleles. This process is counter to predictions from Mendelian genetics and remains poorly understood but can dramatically shorten the cycle in genome-based breeding.

Making Better Use of the Sun

Stephen P. Long

University of Illinois

That the continuous growth in population will exceed crop production has caused fear of global famine since the 18th century but has been averted by a series of technological innovations in farming—most recently the genetic improvements of the Green Revolution. The UN Food and Agriculture Organization predict a 60% increase in crop demand by 2050. But the approaches of the Green Revolution are reaching their biological limits, while global change and declining availability of irrigation water threaten production. Given the 20 years between innovation and availability of new technologies to farmers at scale, we have little time to avoid failure in supply. One crop process that has not been improved is that of photosynthesis: the conversion of sunlight energy into plant matter. Theoretical systems and synthetic analyses of this best known of all plant processes have suggested a number of points from metabolism to organization of leaves where photosynthetic efficiency could be improved (Long et al., Cell 161, 56–66). Today, the first bioengineered demonstrations that these theoretical improvements work in practice in farm settings to very substantially increase yield have emerged. It gives proof of a key means to achieve a much-needed Green Revolution 2.0. Much still is needed to realize this opportunity, but that this is well worth pursuing with urgency is clear.

Coping with High CO₂

Julian I. Schroeder

University of California, San Diego

The steeply rising atmospheric CO₂ concentration is driving climate change, imperiling food security and quality for a growing world population. The entry points for CO2 in plants for photosyn-thesis are stomatal pores on leaves, but their opening causes >90% of plant water loss via evapotranspiration. Plants lose hundreds of water molecules per photo-synthetic carbon atom fixed. Furthermore, elevated [CO₂] in leaves is a signal during dark respiration that causes stomatal closure. Consequently, the atmospheric CO₂ rise is reducing stomatal apertures globally in diverse plants and crops, but to different, non-optimal, degrees.

With [CO2] in the atmosphere already 50% higher than before the industrial revolution, plants theoretically could substantially reduce water loss while not suffering a reduction in photosynthetic carbon fixation. This has been demonstrated in the lab through increasing plant water use efficiency by >40% by upregulating the stomatal CO₂ response in the plant Arabidopsis thaliana. However, the stomatal CO₂ signal transduction machinery remains inadequately understood. Moreover, molecular engineering and breeding in different crops will show which plants can most benefit from tuning the stomatal CO₂ response for improving water use efficiency in drought-prone agricultural regions. On the other hand, for plants grown in water-abundant environments, reducing the stomatal CO₂ response, together with other improvements, could also become relevant for boosting carbon intake and yields in a high-CO₂ world.