A genetically modified rice with more starch in its grains also provides fewer nutrients for methane-producing soil microbes. This dual benefit might help to meet the urgent need for globally sustainable food production. See Letter p.602
Despite being much less abundant in the atmosphere than carbon dioxide, methane has a higher capacity to absorb heat emitted from Earth's surface, and thereby contributes substantially to global warming1. The demonstration2 that reducing emissions of this greenhouse gas can be achieved more easily and more rapidly than for CO2 has spurred an avalanche of studies on possible methane-mitigation strategies. Rice cultivation is the largest single source of methane linked to human activity, and methane emissions from rice paddies are expected to increase with a rising global demand for food. On page 602 of this issue, Su et al.3 describe a 'high-starch, low-methane' rice variety that represents a tremendous opportunity for more-sustainable rice cultivation.
In rice, the leaves and stems take up CO2, which is transformed through photosynthesis into sugars that are used to produce plant biomass or storage compounds, such as starch, in the shoots, roots and rice grains. Carbon from decaying roots or that is directly released by roots into the soil in the form of sugars, amino acids and organic acids, can be transformed by decomposer microorganisms into substrates (CO2, hydrogen and acetate). In the absence of oxygen, these substrates are turned into methane by methanogenic microorganisms. The methane can remain in the soil, escape to the atmosphere through diffusion into and emission by the rice plants, or be intercepted by methane-consuming bacteria in the root zone or the soil's surface layer. These bacteria use methane as a substrate for oxygen-requiring respiration, producing CO2. Hence, methane emission from rice soils is determined by the balance of methane-producing and methane-oxidizing microbes, the availability of other substrates, and the activity of microbes competing for these compounds — collectively, these processes constitute the methane cycle (Fig. 1).
Existing efforts to mitigate rice-associated methane emissions have focused mainly4 on agricultural practices — such as water management, fertilizer use, tillage and crop selection — that alter the environmental conditions for methanogenic microorganisms. However, these measures are labour intensive and their applicability varies between rice-cropping systems and between countries. In 2002, it was observed5 that the larger the amount of grain carried by the rice plants, the less methane is emitted, because carbon fixed in the grains does not become available for soil microbes to turn into methane. This observation suggested a globally applicable methane-mitigation solution: produce a rice plant with a higher proportion of its carbon in the stems and grains than current varieties. Crops of this plant would not only result in less methane emissions, but also give higher grain yield and higher nutritional value. But it has taken until now for such a plant to be generated. Su et al. present evidence from field and greenhouse trials of varieties of transgenic rice called SUSIBA2 that fulfil these criteria.
The authors generated their rice varieties by transferring genes from barley that are responsible for the production of starch in stems and grains; in rice, these genes lead to higher starch production, and hence a higher demand for sugars, in these plant parts. The transgenic rice displayed the expected properties of higher seed weight and higher starch content in seeds and stems, but no change in starch levels in leaves and roots and a markedly lower root biomass. By screening the expression of a large set of genes involved in converting sugar into starch, the authors confirmed that the inserted genetic elements were effective only in the seeds and stems.
The 'cherry on top' of these genetic efforts was a significant reduction in methane emitted from SUSIBA2 rice plants, compared with a widely grown unmodified variety. The methane was measured by covering the plants with transparent gas-collection chambers. A decrease in methane emission was seen in trials of two variants of SUSIBA2 rice in three regions of China, measured in three consecutive growing seasons. The authors also found fewer methanogenic microorganisms on and around the roots of SUSIBA2 rice, suggesting that there was less plant-derived carbon-containing substrate available for methanogens.
Although Su and colleagues have made the groundbreaking demonstration that high-starch, low-methane rice plants can be generated, their study raises many issues. The most obvious is that SUSIBA2 rice is a transgenic plant, and thus raises biological and ethics concerns. In addition to the general questions surrounding the use of genetically modified crops for human consumption, and how access to seed for such crops is controlled, we do not yet have a clear picture of how this modification affects rice plants' survival and general function.
Long-term and frequent measurements of methane emissions from areas planted with normal and transgenic rice are needed to estimate what the annual global effect of the widespread use of this crop would be, and how it compares with that of other methane-mitigation strategies. Even more important will be assessment of the long-term consequences of lower carbon and oxygen input by the roots of SUSIBA2 plants on soil processes and the microbes that carry them out (Fig. 1). It has recently been shown6 that highly specific assemblages of microbial species occur in, on and around rice roots, and that not all members use plant-exuded carbon7. Long-term reduction of root-exuded carbon might alter the composition of these communities, with unknown consequences for microbes that are plant pathogens or that benefit the plants, such as the bacteria that decompose organic material and deliver essential plant nutrients8.
To compensate for the possible reduction in plant nutrients, larger amounts of nitrogen fertilizer would need to be applied. This can affect both methane producers and consumers9 and lead to undesirable environmental effects, such as nitrate leaching to groundwater and emission of the potent greenhouse gas nitrous oxide. Also crucial for the amount of methane emitted is the activity of methane-consuming aerobic bacteria. The oxygen they use flows though the plant stems and roots into the soil by the same route taken by methane moving out of the soil into the atmosphere, and it is not known how the transport of gases is affected in the transgenic rice.
Thus, translocating more carbon to the stems and seeds of SUSIBA2 rice may bypass methane cycling, but this activity has the potential to affect a multitude of processes involving soil carbon, nutrients and microbial activity, with knock-on effects for the sustainability of rice cultivation. However, Su and colleagues have achieved the feat of making high-starch rice available, and this will spur scientists worldwide to conduct experiments to verify whether this variety will enable more-sustainable cultivation of the crop that feeds half the human population.
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Ecological Processes (2017)