Challenges of translating Arabidopsis insights into crops

Abstract

The significance of research conducted on Arabidopsis thaliana cannot be overstated. This focus issue showcases how insights from Arabidopsis have opened new areas of biology and directly advanced our understanding of crops. Here, experts intimately involved in bridging between Arabidopsis and crops share their perspectives on the challenges and opportunities for translation. First, we examine the translatability of genetic modules from Arabidopsis into maize, emphasizing the need to publish well-executed translational experiments, regardless of outcome. Second, we highlight the landmark success of HB4, the first GM wheat cultivar on the market, whose abiotic tolerance is borne from direct translation and based on strategies first outlined in Arabidopsis. Third, we discuss the decades-long journey to engineer oilseed crops capable of producing omega-3 fish oils, with Arabidopsis serving as a critical intermediary. Fourth, we explore how direct translation of starch synthesizing proteins characterized in Arabidopsis helped uncover novel mechanisms and functions in crops, with potential valuable applications. Finally, we illustrate how shared molecular factors between Arabidopsis and barley exhibit distinct molecular wiring as exemplified in cuticular and stomatal development. Together, these vignettes underscore the pivotal role of Arabidopsis as a foundational model plant while highlighting the challenges of translating discoveries into field-ready, commercial cultivars with enhanced knowledge-based traits.

Figure 1.

From translation to interpretation: growth processes as an example and recommendations for the future. A) In leaves, the growth processes of cell division and cell expansion are, to a certain extent, similarly regulated in dicots and monocots; for several pathways, orthologous genes are present in both Arabidopsis and maize. However, we currently lack an understanding of why similar genetic perturbations in Arabidopsis and maize sometimes lead to comparable phenotypic outputs (as seen with GA20OXIDASE, CYP78A, and GIF1), while in other cases they do not (e.g. SAMBA, DA1, DAR, and BB). B) Recognizing these “negative” translational outcomes and gaining insights into the potential reasons for these differences in “translatability”—such as differences in penetrance, physiology, anatomy, redundancy, or network rewiring—will be critical. C) Making data from well-executed experiments with lack of phenotypes available will serve meta-analyses and allow to incorporate this understanding into the design of future model-to-crop experiments to significantly enhance the ability to translate plant biotech research into practical applications. Created in https://BioRender.com.

Figure 2.

Schematic representation of the pipeline to follow to translate molecular technologies from Arabidopsis to crops. Schematic and abbreviated steps to be followed from gene discovery to arrive at a market product. Triangles indicate the way forward when there are beneficial effects. In the central square: illustrations of such steps and experiments needed to decide progress. The characteristics to be evaluated at each stage are shown in the bottom rectangles. Crosses for each characteristic indicate detrimental effects, determining the need to backtrack following the arrow.

Figure 3.

Schematic representation of engineering plants to accumulate omega-3 polyunsaturated fatty acids by the addition of genes from marine microalgae. Representative sources of biosynthetic genes are shown (from left to right: Phaeodactylum tricornutum; Mantionella spp.; Emiliana huxleyi; Thalassiosira pseudonana). Codon-optimized open reading frames encoding the enzymatic activities required for the synthesis of EPA and DHA were expressed under the control of seed-specific promoters and introduced into Camelina sativa by Agrobacterium-mediated transformation. The ability of Camelina to be transformed by floral dipping facilitated direct translation from studies in Arabidopsis.

Figure 4.

Starch granule morphology observed using scanning electron microscopy. Arabidopsis produces starch in its leaves, and the starch granules are relatively small and have a flattened appearance. In the endosperm starch of cereals, there is vast natural variation in granule shape and size. Wheat starch has distinctive bimodal granules that can be further classed into large A- and small B-type starch granules (marked in the figure). Variation in granule morphology can be induced in wheat by mutating granule initiation genes characterized in Arabidopsis. Bars = 20 µm.

Figure 5.

Complementary research in Arabidopsis and crops aids understanding of epidermal features in plants and the engineering of plant surfaces for improved crop performance. The outer epidermal cell layer is covered by cuticle and made up of mostly pavement cells interspersed with other specialized cell types. In Arabidopsis, specialized epidermal cells are scattered across the leaf surface, while in cereal grasses such as barley, epidermal cells are arranged with pavement cells in distinctive files. In both cases, specialized cells are spaced away from each other. Cuticles can vary by cell type and also show specializations between species, such as crystalline wax blooms in barley. Research on Arabidopsis greatly informs our understanding of genes and pathways guiding epidermal cell spacing and cuticular metabolism in crops and together reveals extensive conservation but also variation and novelty across species. Excitingly, complementary research in both Arabidopsis and grass models paint an emerging picture of how the regulation of cuticular specializations and epidermal patterning may be coordinated. Leveraging these insights will help us better engineer crops for desired epidermal traits. SEM photos present wax blooms on the leaf sheath of barley. Scale bar = 5 µm.