Matthew Paul of Rothamsted Research describes recent developments in breeding higher yielding, stress-resilient crops able to withstand the effects of climate change.
Introduction
The Green Revolution of the 1960s and 1970s was a major technological achievement. Yields of wheat and rice increased substantially due to the incorporation of alleles for reduced stem height and for resistance to rust diseases[1].
This resulted in an estimated saving of a billion lives in Asia. It turned previously net importers of grain into net exporters over the course of a few years. However, the period of low and stable grain and food prices during the latter part of the 20th century came to an abrupt halt in the first decade of the 21st century, which saw at least one food crisis year, accompanied by food price increases due to poor harvests in different parts of the world.
This has reawakened interest in the importance of food security and highlighted the need for higher yielding resilient crops.
Crop yield potential and resilience and the need to increase them together
The food crisis of 2008 was due to the combined effects of poor weather conditions on yields and progressively stagnating yields. Currently, the rate of yield improvements of the major crops is behind that required to meet the demands of the predicted global population in 2050[2]. Unless crop yields are increased above the current trend line of around 1% per annum for major food security crops (wheat, rice and maize) to well above 2%, then food shortages are likely to become more prevalent as the century progresses. Yield potential of crops needs to be increased, but this should be combined with resilience to environmental stresses, particularly drought and heat. This is a current grand challenge for agriculture.
Currently, the rate of yield improvements of the major crops is behind that required to meet the demands of the predicted global population in 2050.'
Climate change
Two main effects of climate change, increasing temperature and altered rainfall patterns, are predicted to reduce crop yields. Additionally, there is the likelihood of extreme event scenarios, also expected to have a negative impact. Increasing CO2 levels may have a beneficial effect on photosynthesis, but interestingly this is not being seen in global trends of crop yields e.g. the plateauing of wheat yields in the UK since 1995[3].
This would suggest that the benefits of increasing photosynthesis due to year-on-year increase in CO2 levels, now accelerating at 3 ppm per year, are quite minimal and that limitations to yield lie elsewhere. Global temperatures have risen by 0.5°C in the last 50 years (NASA climate data). For every 1°C increase in temperature, there is a yield loss of wheat (6%), maize (7.4%), rice (3.2%) and soybean (3.1%)[4]. Changing rainfall patterns may lead to more unpredictable droughts. Drought is already the major widespread abiotic factor that limits global crop yields.
Improving crop yields for the 21st century
Increases in yield potential need to be combined with resilience to a mix of abiotic stresses. However, this is some task as mechanisms of productivity do not necessarily overlap with mechanisms of stress resilience.
Mechanisms of resilience in the natural environment are more about survival than about high yield. There are examples of genes that confer tolerance and survival of drought, which have been transferred by genetic modification; these produce plants that perform and survive better under drought, but grow less well under full irrigation. This is not an acceptable compromise[5]. Hence an important goal is to combine improvements in drought and heat tolerance with improvements in overall yield potential under optimal conditions.
Forward and reverse genetic approaches
Conventional breeding has succeeded in feeding world populations, but yield improvements through this route are currently slower than required to meet projected population growth. Ways of speeding up yield improvements are required. Usually the genetic and physiological bases of yield improvements are unclear. This means that more directed and targeted breeding with markers is not possible.
To speed up the breeding process, crop improvement can start from a forward or reverse genetic approach (Figure 1). With the ability to clone genes, reverse genetics became a popular way to understand the functions of specific genes through the creation of knockouts or over expressers in transgenic plants. This has been a very powerful means to understand gene function in the context of whole plant physiology, often termed molecular physiology. It was thought that transgenic crops for enhanced yield and resilience to abiotic stresses would soon become common place in agriculture. However, despite GM crops having been extremely successful for traits, such as insect pest resistance and herbicide resistance, yield and abiotic stress resilience have been far less amenable to improvement by GM. This is often because we do not know the yield or drought genes to target. Additionally, yield and abiotic resilience are complex multigenic processes, hence simple changes are not likely to produce positive outcomes unless master regulator genes that regulate other genes can be identified[6].
Forward genetic approaches seek to find genes associated with improved traits so that in the absence of other selection methods, genetic markers could be developed to enable more rapid screening of germplasm. However, genomics assisted selection has not yet contributed much to the improvement of stress tolerant varieties. Sequence-based DNA markers, notably single nucleotide polymorphisms (SNPs), are gaining popularity and are expected to advance the dissection of complex traits on complex genomes due to their high linkage with heritable variation[7]. The regions within genomes that contain genes associated with a quantitative trait are known as quantitative trait loci (QTLs). The full benefits of molecular markers in selecting for quantitative traits is still challenging as most marker techniques are just qualitative measures indicating the presence of a gene with no information on levels of expression and its integration with genetic and regulatory networks. It is necessary therefore to integrate molecular tools with precise high-throughput phenotyping and biochemical analysis to confirm the consistency of molecular markers. Detection of QTLs containing the genes conferring quantitative traits, including drought tolerance, have revolutionised the selection process towards marker assisted and genomic selection. Time will tell if this results in significant improvements in the rates of introduction of new varieties.
Additionally, attempts are being made to increase the genetic diversity of major crops. The National Institute of Agricultural Botany in Cambridge has recreated the original rare cross between an ancient wheat and wild grass species that happened in the Middle East 10,000 years ago. The result is a ‘synthetic’ wheat which, when crossed with modern UK varieties, could offer new sources of yield improvement, drought tolerance and other traits. The synthetic hexaploid wheat breeding programme re-captures some of the variation from those ancient wild relatives lost during the domestication of wheat as agriculture evolved.
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| Figure. 1. Forward and reverse genetic approaches used in the development of new crop varieties |
Breeding for drought
The International Maize and Wheat Improvement Center (CIMMYT) has provided wheat varieties adapted to marginal environments, which have been adopted globally through multi-environmental testing and collaboration with international breeding programmes[8].
However, the rate of yield increase is still too low to catch up with the projected 70% increase in demand for wheat by 2050. Much of the yield increase under drought is likely to result from spill over benefits of selection for yield improvement under good growing conditions e.g. reduced plant height.
The flowering period is a growth stage particularly sensitive to drought. Delayed silking is a side effect of drought and is commonly used for selection in breeding approaches to drought tolerance for maize. In wheat, reduced number of days to anthesis and maturity enables the crop to evade terminal drought. Leaf width has proved to be a good selection parameter for early vigour to increase water use efficiency because evaporation of water from the ground is reduced due to the faster establishment of leaf canopy[9]. This is important in regions with Mediterranean-type climates. Root angle is a common trait for selecting drought-tolerant phenotypes, where the root angle directly influences root distribution in the soil allowing for deeper roots to develop and find water.
Wheat traits of reduced evaporative losses and maintenance of assimilate production, seen in leaf rolling and flag leaf persistence, are used as selection parameters. Several phenotypic drought-responsive traits in wheat have been correlated with molecular markers allowing precise mapping of their respective quantitative trait loci (QTLs) on chromosomes. However, QTL identification for tracing drought tolerance remains a challenge due to the large number of genes influencing the trait, instability of some QTLs, the large size of the wheat genome and epistatic QTL interactions. To date, several putative QTLs for drought tolerance-related traits have been mapped in wheat, particularly on the A and B genomes.
Stable carbon isotope (13-C) analysis is an important method of assessing plant responses to environmental stress, especially drought[10]. Plants discriminate against 13-C during photosynthesis, resulting in a lower 13-C isotopic composition in plant tissue than in the atmosphere. Studies have shown that the degree of discrimination against 13-C is determined largely by intercellular CO2 concentration, which is controlled by the ratio of photosynthesis to stomatal conductance. Stable carbon isotope discrimination may be used to estimate water use efficiency over the crop life cycle integrating physiological responses over time rather than presenting a series of ‘snapshot’ measurements.
Graham Farquhar and Richard Richards from the Australian National University and CSIRO in Australia showed that variation in the carbon isotope composition of different wheat types was correlated with water use efficiency. They screened the leaves of different wheat strains to determine the ratio of carbon-13 to carbon-12 and identify the plants that had higher water use efficiency. They suggested that this carbon isotope analysis could be used to select water efficient wheat varieties in breeding programmes.
Wheat varieties with low carbon discrimination were identified and crossbred with wheat of good quality grain and yield to produce a strain that could use water more efficiently. The researchers succeeded in producing the first commercial wheat varieties to be bred using gene selection techniques that had improved yield for the same amount of water. The first varieties, called Drysdale wheat and Rees wheat, were specifically designed for dry environments like Australia.
These wheat varieties were very successful and the technique of identifying water efficient plants using stable isotopes of carbon has also been applied to other crops, such as rice and barley.
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| Figure 2: Scanalysern field phenotyping platform at Rothamsted Research used to measure crop growth, development and performance at field scale |
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| Figure 3: Genetic variation displayed in winter wheat plots at Rothamsted Research |
GM of drought tolerance
The only commercially available drought-tolerant crop that constitutively overexpresses the Bacillis subtilis cold shock protein B (CspB) is maize. This improves plant performance under drought imposed during vegetative as well as reproductive development. CspB gene expression stabilises plant RNA and helps plant cells to produce proteins that are essential for growth, which supports yield formation when water is scarce. Transgenic plants produced more chlorophyll and had higher photosynthetic rates. The commercially available CspB maize trait improved grain yield by 6% when water-deficit was imposed at mid-vegetative to mid-reproductive stages in multi-year field testing[11].
Recently, GM, again of just one gene but this time using a developmental promoter rather than a constitutive promoter to control gene expression, has resulted in even larger improvements in yield under drought in maize. Drought during the flowering period can result in the abortion of developing kernels due to impaired sucrose supply. Expression of a trehalose phosphate phosphatase (TPP) gene under the control of a MADS6 promoter, expressed only in reproductive tissue during the flowering period, results in more sucrose in kernels reducing kernel abortion. It is thought that trehalose 6-phosphate (T6P) is a key regulatory metabolite that determines the use and allocation of sucrose at the whole plant level.
By changing T6P abundance with the TPP gene, which encodes a phosphatase enzyme that metabolises T6P, it is thought that a starvation signal is generated by lower abundance of T6P, which results in more sucrose import into the kernels. It is likely that T6P is a master regulator and regulates many genes that determine sucrose use and allocation in crops, a process central in determining yield and resilience. Maize plants with this genetic change were 9-49% higher yielding under mild or no drought conditions and up to 123% higher yielding under more severe drought[12].
Interestingly, a TPP gene has also been shown to underpin a QTL responsible for germination of rice under flooding anoxia[13]. In this case TPP enables better mobilisation of starch reserves required during germination under flooding. This means that rice can be directly seeded rather than transplanted saving the drudgery and labour-intensive process of transplanting rice plants to flooded fields. A convergence of different traits around one regulatory pathway centring on T6P means that this pathway may have great potential as a target in crop yield enhancements for different environments.
Heat stress
As with drought tolerance, heat stress tolerance is a complex multigenic trait. An increase in temperature leads to faster development, shorter crop duration and hence less light interception and assimilation during the life cycle; it also increases maintenance respiration rate meaning less carbon is available for yield formation. More extreme heat during flowering can limit fertility, impairing pollen viability and meiosis[14]. The same constraints for improving crop resilience to drought apply to heat.
More knowledge is required about the fundamental science of which genes could be targeted for yield improvement. It is possible that similar mechanisms could protect against both heat and drought. This will be useful as heat and drought often occur together.
It may be that improvements in carbon use and allocation found to improve performance under drought and flooding could also be targeted for improvements in heat tolerance i.e. increased allocation of sucrose to reproductive structures and slower consumption and respiration of sucrose at higher temperatures.
Conclusions
The development of agriculture and the crop yield improvements of the 20th century have led to and sustain civilisation over much of the globe. Poverty and food shortages are still problematic but could be addressed through further improvements in crop yields. This is particularly important given continuing population growth and climate change predicted over the next 50 years.
For real advances in the production of higher yielding, stress-resilient crops, there needs to be a coming together of different disciplines and sectors of crop research. For example, research on the understanding of the fundamental crop processes that limit yields often conducted in universities and institutes should be combined with phenotyping and the large-scale field trialling facilities of the private sector. Genetic resources should be shared and closer collaborations set up between institutions.
Genetic variation and the power of genomics, coupled with application of knowledge of the processes and underpinning genes that limit yields in the agricultural system, would be the route to the delivery of a second green revolution for the 21st century.
Dr Matthew J Paul, Plant Science, Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK
Guest Professor NEF University, Harbin, China
Email:matthew.paul@rothamsted.ac.ukTel: +44 1582 938230
Web:https://www.rothamsted.ac.uk/our-people/matthew-paul
References
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