An archaeogenomic approach to maize evolution, adaptation, and biodiversity in North America

Lead Research Organisation: University of Warwick
Department Name: School of Life Sciences

Abstract

Maize (or corn, Zea mays) is one of the most important crop plants worldwide. It is grown on six continents, is one of the top three staple crops for human consumption, feeds livestock worldwide, and helps fill a growing demand for ethanol-based fossil fuel alternatives. Maize adapts readily to diverse environments, and as a result, it is grown in an incredible range of ecological settings, making it a valuable asset to global food production and food security. This remarkable level of biodiversity is due in part to an abundance of transposable elements (TEs) in the maize genome; short, non-coding regions of DNA capable of rapidly altering the genome at a structural level by self-propagating throughout the genome and interrupting normal DNA replication. The resulting random alterations to the genome can be detrimental to the host organism, but can also introduce variation that is beneficial in certain evolutionary contexts. TE replication occurs in episodic bursts rather than at a predictable, steady pace, and these episodes are known to occur as a direct result of environmental stressors, such as those encountered when a domestic species is introduced to an unfamiliar habitat. In sum, when maize is introduced to a new habitat with environmental conditions such as low rainfall, a short growing season, or high altitude, these stressors can drive a surge in TE activity that rapidly introduces an abundance of random variation into the genome. Some of this variation could alter genetic pathways in ways that confer an advantage in the new habitat. Such variation would be extremely beneficial to the population, and under human cultivation, would rapidly be propagated throughout the crop fields by artificial selection. We believe that much of maize's robust adaptation to diverse habitats is driven by this process.

The origins of maize can be traced to teosinte, a wild tropical grass native to Mexico that bears little resemblance to the familiar crop plant, but was being acted upon evolutionarily by human use and selection beginning 7,000-9,000 years ago (BP). Teosinte is not terribly useful to humans in its wild form, but selection for a few key traits early in the domestication process made it a high-yielding and robust crop plant. By the time Europeans arrive in the Americas, extremely diverse and well-adapted landraces were being intensively cultivated throughout the New World.

Maize was carried northward out of Mexico to the American Southwest around 4100 BP, where it came to form an important part of the local diet. Around 2100 BP, maize was brought into eastern North America, but it made no significant dietary contribution until 1100 BP, when it suddenly became the dominant crop of the Eastern Woodlands, and was involved in major social and political changes occurring in the region. We suggest that maize underwent a period of local evolution driven by TE activity after arriving in eastern North America, without which the introduced southwestern varieties would have been unsuitable for such broad-scale agricultural intensification a thousand years after their arrival. We propose to isolate and analyze ancient DNA from archaeological eastern North American maize to identify patterns of TE activity suggesting adaptation to local conditions, and modern genomic methods with North American landraces to identify candidate genes that might have been affected by TE activity, and that therefore might have been involved in local adaptation. In addition, we propose to grow southwestern maize varieties in a simulated eastern North American environment to test whether TE activity is inducible by the inherent ecological stressors placed on non-local landraces. Our study will help us understand the fundamental mechanisms underlying biodiversity in one of the world's most important crop plants, a prospect with profound implications for global food security and ecosystem health in the face of climate change and declining crop biodiversity.

Planned Impact

Beneficiaries of the proposed research:
The most direct beneficiaries of this work are as follows: 1) Crop scientists interested in the genomic bases of phenotypic evolution in maize; 2) researchers studying major changes in the ecological and social landscape accompanying agricultural intensification; 3) private sector and policy-based interests focused on sustainable biodiversity in commercial maize production, especially in the climate of major agri-business' dominance of the industry and push away from diversity in crop fields; 4) the growing field of diverse environmental 'omics researchers in the UK and abroad, and in particular, researchers seeking to integrate computational genomics and advanced bioinformatic tools into archaeogenomic and environmental genomic applications.

How these groups will benefit:
1) Crop scientists seeking to develop and improve varietal maize in any eco-region will benefit from a more comprehensive understand of the biological processes that underlie maize's adaptive response to external stimuli, including new environments and artificial selection pressures. Our research will highlight the fundamental genomic underpinnings of variation in maize, especially as they pertain to its ability to thrive under ecological scenarios of extreme diversity. Our findings, therefore, will have the potential to influence crop scientists' approach to manipulating maize phenotypes in ways to benefit human cultivators.
2) The onset and intensification of agriculture are topics of perennial interest among archaeologists seeking to understand the role of changing food production strategies in societal and human ecological evolution. Reconstructing particular pathways of maize evolution, therefore, speaks directly to the trajectory of this prolific crop as it rose to prominence throughout the New World, and eventually on a global scale.
3) While a growing proportion of the maize grown and traded worldwide represents a genetically homogenous monoculture, it is critical for reasons of food security to vigorously pursue research into maize biodiversity. Commercial maize production with heavy herbicide application-facilitated by genetic modification conferring herbicide resistance-spurs the rapid field-evolution of herbicide resistance in previously innocuous weeds, and has detrimental environmental impacts from a soil- and waterway-pollution standpoint. These strategies for global food production are clearly unsustainable, and a focus on a robust level of biodiversity must be part of the solution. Therefore, governmental and private sector bodies seeking to invest in sustainable alternatives to current strategies of commercial maize production will benefit from a more direct and fundamental understanding of the mechanisms underpinning maize diversity, and can integrate information gained through our research into strategic planning for a more sustainable system of maize production.
4) Finally, our proposed research is highly computational in nature, and will entail the development of advanced bioinformatic tools. These will be curated for user-friendly integration into research pipelines, and will be made freely available to any interested researchers. We feel that our research will help advance the field of bioinformatics among the UK 'omics community, especially in the growing disciplines of archaeogenomics and environmental genomics.
 
Description We fundamentally revised our understanding of maize domestication by combining modern and ancient genomes, in a way that informs the domestication process for other crop species and will help shape the next decade of domestication research. Briefly, we found robust evidence that Indigenous farmers in the Americas began transporting and caring for diverse maize landraces well before the development of robust domesticated forms that we would recognize from present-day agriculture. This sheds light on the importance of even partially domesticated species, and humans' perception of domestication and food security.
Exploitation Route These findings fundamentally reshape our understanding of plant domestication, which is arguably the most impactful process in human history. There is substantial scope for research following on from these findings.
Sectors Agriculture

Food and Drink

Environment

 
Description Warwick SLS Pump Priming
Amount £5,000 (GBP)
Organisation University of Warwick 
Sector Academic/University
Country United Kingdom
Start 03/2015 
End 07/2015
 
Title Ancient DNA profiling 
Description We published a revision of the general model of ancient DNA decay (Kistler et al 2017 Nuc Acids Rec), with several scripts made available for computation of DNA damage statistics. 
Type Of Material Data analysis technique 
Year Produced 2017 
Provided To Others? Yes  
Impact Scripts are available and the work is highly cited, 37 references in the first ~18 months.