ReviewPlant science and agricultural productivity: Why are we hitting the yield ceiling?
Introduction
Plants are the engines of terrestrial (agro)-ecosystems. Primary photosynthetic production sets the absolute upper limit for all heterotrophs and present agricultural production [1]. Plants also sequester carbon, and operate as factories producing diverse chemicals, and plant ecosystems serve as water reservoirs. These properties have been used by humans to produce an extremely productive agriculture in the past millennium.
Domestication by our preliterate ancestors achieved spectacular results, through critical selection of modifications to morphology, physiology, and biochemistry of plants and animals. Further modifications of comparable ingenuity may be required for the needed increases in production (see Section 7). Plant breeding has been historically oriented toward high agronomic yield, disease and pest resistance, easy and consistent processing, and traits advantageous for cultivation and business. In conventional modern agriculture, the Green Revolution is considered “the first systematic, large-scale attempt to reduce poverty and hunger across the world” by substantially increasing production [2]. The recipe for this was an assortment of high yielding, water- and/or fertilizer-responsive varieties, irrigation, pesticides and fertilizer use [3].
What has been the contribution of ag-biotech? A report prepared by a USDA A21 committee shows that yield security is a main target of ag-biotech [4]. The first two classes of products of crop biotechnology, broad-spectrum herbicide-tolerant and Bt-mediated insect resistance crops in corn, cotton, canola and soybeans (i.e., crops with large seed markets), have been widely adopted in the U.S, Canada, South America, India and China because such traits have not been generated through classical breeding. By 2012, more than 10% of the world crop lands were growing transgenic crops, with an annual growth rate of 6% [5]. The new varieties essentially provided increased profitability [6], and, as a collateral benefit, reduced pesticide use and better conservation tillage. Near-term applications offer resistance to viruses, pathogens and insects, and improved processing and storage [7], [8].
Despite such spectacular advances in the past, we now seem to be reaching yield ceilings in several major crops and the increase of global relative crop yields is slowing down [9], [10]. While some local potential for yield increase is recognized in Africa and SE Asia, the fundamental causes of this levelling off include lack of genetic diversity for breeding programs, including the numbers of species used, climate instability, cultural practices, soil and environmental degradation, losses of agricultural land, and economic constraints (and in particular under-investment in agriculture since the end of the 1980s) [3], [9], [11]. For example, today 80% of calories for humans and livestock come from only four species [9]. The need for a second green revolution is advocated by experts [3], [12], and institutions, such as FAO [13], with strong emphasis on research towards: (1) the understanding of mechanisms by which genetic variation, genome architecture, and environmental cues and changes can modify yield; (2) shifting breeding goals towards more environmentally-friendly agriculture. These approaches require a much broader thinking in both science and society than before.
Section snippets
Conventional genetic yield improvement methods in agriculture
Crop productivity presently combines the effects of the domestication and refinement of crops by pre-scientific peoples, along with two centuries of breeding programs, partly informed by genetic knowledge. Both stages in the development of agriculture are important because in both cases humans have affected the strength and the direction of selection. The biggest changes to plant architecture and morphology happened in the former period. For example, maize is so different from its ancestor
The current understanding of bioproductivity – hitting the yield ceiling
Bioproductivity is a key characteristic of biological resources. Productivity is essentially understood and evaluated as production or yield (see supplemental files S1 and S2, summarizing in glossary format the various terms in use). How much harvested biomass one can produce by growing a given genetic material or by a particular biological community in a given environment is what appear to matter most to farmers.
The Food and Agriculture Organization takes the following approach to gauge the
Reframing bioproductivity—integrating the agro-ecosystem ceiling with systems level processes
Plant science is faced with a strong challenge: ensure yield security while shifting breeding goals in order to produce more with less. A global analysis of yield patterns using geospatial data has estimated that by optimizing worldwide potential yields (as realized or attainable yields) of major crops, i.e. by increasing agricultural resource efficiency, global food production could be increased by approximately 30–60% with current agricultural practices and technologies [10]. An OECD-FAO
The biological foundation of plant productivity—three key general processes
Plant architecture is the result of two interrelated processes: the rates and patterns of organ formation at the apex, relative to the rates of growth of organs and internodes. Architecture is important for productivity in multiple ways, such as contribution to photosynthetic and water use efficiencies and to the ability of grain crops to avoid lodging. Plant growth is the direct expression of biomass production, driven by photosynthesis, which primarily depends on light, water, and nutrients.
Mechanistic bases of productivity: key examples
The chosen examples illustrate processes controlling productivity and yield at the levels of the entire organism, the individual organ, and the cell. They also help in understanding what we termed “productivity potential” and the factors that modify its expression (i.e. the realized yield/performance; see Section 4).
A few master (“magic”) genes have been identified as major players in plant productivity, most famously those involved in domestication [18] and those for dwarfing, that were at the
Agro-evo-devo, from domestication to “imaginomics”
The genetic diversity within landraces and wild relatives is mined in traditional crop breeding to find yield-enhancing genes. For some crops valuable genes may now be mined out. This creates a “genetic glass ceiling” that impedes future increases in yield [9], [171]. The advent of genetic engineering, in combination with systems biology, offers novel routes through the glass ceiling (see Section 4) [9], as truly dramatic yield increases may require comparably dramatic changes in crop plants.
Conclusions and perspectives
Biological productivity, often taken for granted, remains elusive for a major reason: we need to understand it as an emergent property of living systems involving multiple levels of organization at the same time (Table 1 illustrates this point and summarizes this review). The notion of bioproductivity has been considered here in a much broader sense than previously. The efficiency of biological processes, the mechanisms generating morpho-functional and metabolic adaptations and diversity are
Note added in proof
Specialized membrane transporters offer multiple avenues for significant crop improvement (Schroeder et al [196]). These include better resistance to aluminum toxicity and salt toxicity, allowing agriculture on degraded soils, improved resistance against pathogens, and improved absorption of nitrate from soils, for more efficient fertilizer use. Nutritional value for human consumers can also be improved, for example, using transporters that pump iron or zinc into organs consumed by humans.
Acknowledgements
The presented work has been to a great extent inspired by seminars and discussions with colleagues and students participating for the Masters advanced course “Bio-resources and biodiversity” at ENS de Lyon (http://biologie.ens-lyon.fr/masterbiosciences/presentation-des-ue-1/les-ue-europe/biodiversity/). We are thankful to all of them. We are deeply thankful to the anonymous reviewers who guided us through this vast research area and helped us keeping the main facts in the right focus. The
References (196)
- et al.
Need for multidisciplinary research towards a second green revolution
Curr. Opin. Plant Biol.
(2005) Hybridization as an invasion of the genome
Trends Ecol. Evol.
(2005)- et al.
Heterosis: revisiting the magic
Trends Genet.
(2007) Molecular mechanisms of polyploidy and hybrid vigor
Trends Plant Sci.
(2010)- et al.
Crop genome sequencing: lessons and rationales
Trends Plant Sci.
(2011) - et al.
Rarely successful polyploids and their legacy in plant genomes
Curr. Opin. Plant Biol.
(2012) - et al.
Quantifying blue and green virtual water contents in global crop production as well as potential production losses without irrigation
J. Hydrol.
(2010) - et al.
Secondary metabolism: nature's chemical reservoir under deconvolution
Curr. Opin. Plant Biol.
(2005) - et al.
What is the maximum efficiency with which photosynthesis can convert solar energy into biomass?
Curr. Opin. Biotechnol.
(2008) - et al.
The effect of genotype, environment and time of harvest on sugarcane yields in Florida, USA
Field Crops Res.
(2006)
Strategies for engineering C(4) photosynthesis
J. Plant Physiol.
Size control goes global
Curr. Opin. Biotechnol.
The cauliflower mosaic virus translational transactivator interacts with the 60S ribosomal subunit protein L18 of Arabidopsis thaliana
Virology
A plant viral reinitiation” factor interacts with the host translational machinery
Cell
Genome streamlining and the elemental costs of growth
Trends Ecol. Evol.
DNA amounts in two samples of angiosperm weeds
Ann. Bot.
Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant
FEBS Lett.
Cell number counts-The fw2. 2 and CNR genes and implications for controlling plant fruit and organ size
Plant Sci.
Control of organ size in plants
Curr. Biol.
The evolution of plant architecture
Curr. Opin. Plant Biol.
La force du vivant
Nourrir la Planète
Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers
Science
Food security: the challenge of feeding 9 billion people
Science
Radically rethinking agriculture for the 21st century
Science
Genetic Glass Ceilings: Transgenics for Crop Biodiversity
Solutions for a cultivated planet
Nature
Genetic evidence and the origin of maize
Lat. Am. Antiq.
Darwinian Agriculture: How Understanding Evolution can Improve Agriculture
The rice genome structure as a trail from the past to beyond
Genome Dyn.
Adaptive evolution in ecological communities
PLoS Biol.
From crop domestication to super-domestication
Ann. Bot.
Contributions of domesticated plant studies to our understanding of plant evolution
Ann. Bot.
Paleopolyploidy and its impact on the structure and function of modern plant genomes
Genome Dyn.
The evolutionary position of subfunctionalization, downgraded
Genome Dyn.
Protein-protein and Protein-DNA Dosage Balance and Differential Paralog Transcription Factor Retention in Polyploids
Front. Plant. Sci.
Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homologs
PLoS Biol.
Quantitative trait loci for genetically correlated seed traits are tightly linked to branching and pericarp pigment loci in sunflower
Crop Sci.
Resource distribution and the trade off between seed number and seed weight: a comparison across crop species
Ann. Appl. Biol.
Breeding technologies to increase crop production in a changing world
Science
The effects of artificial selection on the maize genome
Science
The evolution of apical dominance in maize
Nature
Plant domestication, a unique opportunity to identify the genetic basis of adaptation
Proc. Natl. Acad. Sci. U.S.A.
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