Review

Revolutions in agriculture chart a course for targeted breeding of old and new crops

See allHide authors and affiliations

Science  08 Nov 2019:
Vol. 366, Issue 6466, eaax0025
DOI: 10.1126/science.aax0025

You are currently viewing the abstract.

View Full Text

Log in to view the full text

Log in through your institution

Log in through your institution

Growing more and better food

Increasing human populations demand more productive agriculture, which in turn relies on crop plants adjusted for high-yield systems. Eshed and Lippman review how genetic tuning of the signaling systems that regulate flowering and plant architecture can be applied to crops. Crops that flower sooner might be adaptable to regions with shorter growing seasons, and compact plant shapes might facilitate agricultural management. The universality of these plant hormone systems facilitates application to a range of crops, from the orphan crop teff to the well-known wheat.

Science, this issue p. eaax0025

Structured Abstract

BACKGROUND

Among tens of thousands edible plants, several hundred are cultivated throughout the world, but fewer than a dozen comprise the majority of consumed calories. The adaptation to cultivation and further improvement of these crops rely on many changes in plant genomes that are continuously selected by breeders to meet the ever-increasing dietary needs of both humans and their livestock. Although many species-specific genetic and trait modifications helped to elevate the major crops above others to feed the world, the majority of both major and minor crops share a history of a few common modifications to plant physiology and growth that sparked agricultural revolutions. These include the quantitative tuning of flowering signals with direct influences on shoot architecture and productivity, the adoption of shorter-stature plants with more balanced growth in fields treated with chemical fertilizers, and the introduction of hybrid seeds to enhance growth and yield and simplify the combining of disease-resistance genes in hybrid crops.

ADVANCES

Two hormonal systems are at the core of the most successful and reoccurring agricultural revolutions: the flower-promoting protein florigen and its antagonist antiflorigen and the growth-stimulating small molecule gibberellin (GA) and its target for degradation, the growth repressor DELLA. The central components of these hormonal systems govern growth among plant organs. Mutations in the founding antiflorigen gene SELF-PRUNING in tomato and its homologs in other crops such as soybean and cotton confer precocious termination of shoots, transforming tall, vine-like plants into compact bushes better suited for large-scale mechanical harvesting. Similarly, a reduction in GA signals converted wheat and rice into shorter-stature crops, which enabled the Green Revolution. However, all these changes were founded on serendipitous discovery of a few alleles, and the narrow genetic basis for these trait modifications demanded further tuning with species-specific quantitative modifiers for the revolutions to be realized. Tools for genome editing can now rapidly generate a wide range of novel alleles and associated quantitative variation that can be selected to fit specific genotypic background or environmental needs. Transferring beneficial classical alleles into new backgrounds through crosses is time consuming and risks also bringing in negative phenotypic effects from linked chromosomal segments. Generation of a novel allele in the desired background can circumvent those problems. Traits regulating GA and florigen are often shared across plant species, whereas traits such as those that control shattering of seeds and pods are regulated in a species-specific manner. We argue that the core hormone systems, including GA and florigen, offer higher chances than other targets to rapidly generate new beneficial variation to improve old crops and enhance the productivity, adaptation, and adoption of many underutilized crops.

OUTLOOK

Rapid and large-scale environmental and social changes require concomitant rapid and large changes in productivity and diversity of our crops. Adaptation of classical crops to new environments would require retuning of their flowering and shoot systems. Shifting human consumption from environmentally draining animal-based foods to a more plant-based diet will require more high-protein crops. We argue that in the short term, more legumes such as beans are the best option, and in such plants targeted changes in antiflorigen genes were and will continue to be key for large-scale production. Adoption of additional underutilized crops with enhanced abiotic resilience and added nutritional benefits would be expedited by targeted manipulations of the genetic systems that were previously exploited for other crops: flowering, stature, and hybrid seeds. To make the most of these systems in a broad range of crops, the technologies that allow genetic manipulation in all of these plants must be a focus of future research.

The revolution of the protein-rich soybean.

Soybeans (left panel) in the wild are tall, vining plants (middle panel, left). Compatibility for agriculture benefited from a compact, bush-like growth habit (middle panel, right) caused by a flowering and shoot architecture mutation. Large-scale production of soybeans (right panel) serves as an example of how genome editing can generate similar modifications in other protein-rich legumes. Photos courtesy of J.-D. Lee (middle panel) and the United Soybean Board (left and right panels).

Abstract

The dominance of the major crops that feed humans and their livestock arose from agricultural revolutions that increased productivity and adapted plants to large-scale farming practices. Two hormone systems that universally control flowering and plant architecture, florigen and gibberellin, were the source of multiple revolutions that modified reproductive transitions and proportional growth among plant parts. Although step changes based on serendipitous mutations in these hormone systems laid the foundation, genetic and agronomic tuning were required for broad agricultural benefits. We propose that generating targeted genetic variation in core components of both systems would elicit a wider range of phenotypic variation. Incorporating this enhanced diversity into breeding programs of conventional and underutilized crops could help to meet the future needs of the human diet and promote sustainable agriculture.

View Full Text