Farm to Genomes: African Rice

Meyer at al., Nature Genetics, 2016

Meyer at al., Nature Genetics, 2016

Rice is one of the most important crops on the planet, responsible for feeding billions of people. Given this global significance, studying rice in different geographies can be useful and aid in harnessing genetic diversity underlying particular traits and adaptations favorable to different environments. African rice (Oryza glaberrima Steud.) is mainly grown in sub-Saharan Africa and known for its stress tolerance. In a new article this week in Nature Genetics, Michael Purugganan and colleagues report the whole genome re-sequencing of 93 African rice landraces from various regions of Western coastal and sub-Saharan Africa. They create a genome-wide SNP map and through comparative genomic analysis study the domestication and population history of African rice. They use their map to perform GWAS for salt tolerance and find 11 significantly associated regions, highlighting the value of this unique genetic resource.

Meyer et al., Nature Genetics, 2016

Meyer et al., Nature Genetics, 2016

By studying various regions with distinct environments, the authors were able to get clues about adaptation and geographic spread of the populations. They focused on coastal Senegal and inland Togo, which have higher and lower levels of soil salinity, respectively, and interviewed farmers in the region to understand the agricultural practices they employ in each region. The knowledge of the farmers helped to inform the genetic analysis and contributed to the model of African rice domestication and dispersal.

You can watch some of the interviews with the farmers here:

African rice farmers- interviews

Additionally, we spoke with authors Michael Purugganan and Rachel Meyer to get some background on this research.

Why do you think that rice is understudied in Africa compared to other places?

MP: I think it’s because it is not widely grown, unlike its Asian counterpart which has pretty much taken over the world.  But there definitely is more interest in African rice as breeders are trying to figure out how to increase food production in Africa, as well as to try to see what genes in African rice can be used to improve Asian rice.

RM: There is a lot of great research on improving Asian rice for African farmers that is being done by brilliant AfricaRice scientists, and they are working hard on the social science side too. But there are so many challenges that Africa disproportionately faces – particularly climate variation – that demands ramping up rice research. There is insufficient support for programs that integrate crop experiments and trials into the different farmlands. A better connection between scientists and small-scale farmers would really help farmers adopt new varieties too- because there is sometimes resistance to trying new ones.

How did you choose which samples to include in your analysis?

RM: Recognizing that a lot of NGO work encouraging farmers to grow Asian rice ramped up in the 80’s and 90’s, we took advantage of the germplasm largely donated in the 70’s to the West Africa Rice Development Association, which were duplicated and available through IRRI (International Rice Research Institute). We chose accessions with the most metadata available, preferring ones with georeferenced location and a cultivar name. It wasn’t until later that we realized water tables far inland were high in salinity, so we just tried to make sure we had a fair number of samples within 250km of the coast, or along rivers connecting to the ocean.

Were you surprised by any of your findings?

MP: There definitely were a few surprises in the data, but the big revelation for me was the long time for the population bottleneck that led to domestication.  We found from the genomic data that it may have taken more than 10,000 years of steady population decline before full-blown domesticated African rice shows up in the archaeological record.  This suggests the possibility that humans were already cultivating or managing its ancestor for thousands of years, and I think if this pattern holds for other domesticated crop species it will change our thinking on how domestication has taken place.

RM: I was surprised we got nice GWAS results with so few samples, and even more surprised that we saw several of those exhibiting signatures of geographic selection. We were lucky to find a broad distribution of traits in the landraces we chose to sequence, for we had made the DNA libraries ahead of the phenotyping experiments.

What was it like to meet and talk with the farmers?

RM: It was one of the highlights of my life to meet the farmers! I’m grateful to have gotten a glimpse of their heritage, their pride, and their struggles. We were all so impressed with the generosity of women, in particular, to help each other. We were also shocked by how many farms are run by the elderly; their children don’t see farming as profitable and many have left. For the three of us in the field, it made us think hard about how we can give back to the communities that gave us their time. I hope that crop science, publicity (like this blog) and policy changes can raise the profile of the small-scale farmer.

In each interview, the farmers also had a chance to interview us, and that part was especially interesting. Several asked really good questions about African and Asian rice domestication. You could see the cultural value of the basic science.

You chose to focus on salinity tolerance as a trait particularly relevant to farming in Africa.  In what ways do you see your results being used for crop improvement?

RM: One of the authors, from AfricaRice, Dr. Kofi Bimpong, had actually been working on salt tolerance separately as well, and has two graduate student collecting African rice landraces in Casamance. If from this paper we can consider that domestication possibly occurred in the Inner Niger Delta region and also in the West, then these collecting efforts are all the more important because they are from a center of origin, promising more genetic variation than people would have ever estimated. If you look through the available germplasm there is so little that has been collected or studied from Casamance. It’s tricky collecting there, for there is social unrest, and landmines. Hats off to the young graduate students, Mamadou Sock and Bathe Diop, doing that fieldwork; I’m sure there is a lot of discovery to be made with those collections, and more promising salt tolerant landraces to integrate into breeding programs.

In addition, our results suggesting many of the salt tolerance genes are shared in both rice species make them more valuable to explore in other crops.  Shared adaptive mechanisms are especially fascinating to evolutionary biologists and are powerful assets of the breeder’s toolbox.

April issue cover: What’s going on here?

Tlalcacahuatl gold by Erin Dewalt

Tlalcacahuatl gold by Erin Dewalt

This month’s cover image is a visual tribute to the peanut and its importance to both the ancient civilizations of the Americas and modern agriculture. The genome sequences of the two progenitor species to the cultivated peanut were published in this month’s issue by David Bertioli and colleagues. The genome sequences are the first step to characterizing the genome of cultivated peanut, which was formed by the hybridization of these two species thousands of years ago. The genome sequences give us valuable clues about the evolution of these species. The authors also identified candidate genes for pest resistance, which could lead to advances in peanut cultivation in the future.

The image was inspired by a gold and silver necklace with beads in the shape of peanuts that was found in the tomb of the Great Lord of Sipan of the ancient Peruvian Moche culture. The necklace (c. 300) is now at the Museo Arqueológico Nacional Brüning in Peru. You can see an image of the necklace here and with more context here. The peanuts in the cover image have the same wavy shape as the beads in the necklace. The speckled texture and symmetric division of gold and silverish-blue in the cover image are also inspired by this ancient artifact.

Erin Dewalt, senior graphic designer for Nature Publishing Group, developed the image concept. She shows the peanuts underground, almost dangling from the plant above like beads. Peanut seeds develop underground after the flowers are fertilized. The ovary develops into a “peg” (gynophore) that drives back down into the soil, where it develops into the fruit that we cultivate as peanuts.

640px-Arachis_hypogaea_006

Peanut pegs growing into the soil. The tip of the peg, once buried, swells and develops into a peanut fruit. {credit}H. Zell via Wikimedia Commons{/credit}

The title of the image, Tlalcacahuatl gold, is a reference to the ancient Aztec name for peanut, tlalcacahuatl. But it is also a reference to the wealth represented by the peanut, both for ancient cultures and for modern agriculture. Because peanut plants fix nitrogen, thanks to the symbiotic bacteria in their root nodules, they return nutrients to the soil and improve cultivation of other crops (a fact famously advertised to farmers in the U.S. by George Washington Carver).

Tangential reading: The peanut necklace of the Great Lord of Sipan was almost lost to history forever. As this LA Times article from 1988 reported, grave robbers nearly made off with the treasures of the Lord of Sipan, including the necklace.  

 

How we built a better tomato

One species of wild tomato, Solanum lacerdae

One species of wild tomato, Solanum lacerdae{credit}Sandy Knapp{/credit}

Most wild tomato species bear little resemblance to the large, red fruits you’re used to seeing in the supermarket. This is because humans have been molding the tomato to their own taste for thousands of years, by selecting for larger, tastier and (of course) redder fruits.

As a consequence of this selective breeding, we have significantly altered the tomato genome. A new paper published online this week in Nature Genetics analyzed the genomes of 360 tomato accessions, including multiple wild species and cultivated varieties, to understand exactly how and where humans have left their mark on the tomato genome.

This study, the product of a collaboration between many groups around the world, found that human selection on the tomato has led to vast improvement in certain traits at the cost of dramatically reducing genetic variation in large swaths of the genome. An unintended consequence of historical selective breeding in tomato is that there is now little room for improvement on many traits that we care about. By identifying these regions, the study will allow tomato breeders to make more strategic plans for future crop improvement.

We asked one of the study’s senior authors, Sanwen Huang, to tell us a little more about the work and why it is important:

This study was obviously a huge undertaking. How did collaborations come about, and what were the major difficulties in the project?

As an international consortium, we sequenced the tomato genome together (Nature 2012) and this project was regarded as another milestone of tomato research. The difficulty in the current project was deciding what to sequence. Fortunately, our team includes experts who understand tomato germplasm and they studied the natural variation of tomatoes for a long time. As a corollary, we combined tomato lines from many well studied core collections from several countries, such as the US (Roger Chetelat), Israel (Dani Zamir), France (Mathilde Causse), Italy (Andea Mazzucato), and China (Yongchen Du, Zhibiao Ye, and Jingfu Li).

What do you see as the most important aspect of your study’s results?

There are several important results that came out of this work. First, the evolution of tomato fruit size had two stages, from the wild progenitor of the modern cultivated tomato, Solanum pimpinellifolium, to cherry tomato (from ~1g to ~10g), and from cherry tomato to big-fruited tomato (from ~10g to ~100g). We found that there are two independent sets of QTLs or genes that have been selected during the two evolutionary stages. Second, there is a huge genomic signature of the divergence between fresh tomato and processing tomato [tomatoes used for commercial canning], on chromosome 5. This genomic region harbors several genes related to higher soluble solid content and fruit firmness that were selected during breeding for processing tomato. And more interestingly, we noticed that in recent fresh tomato F1 breeding, this region was also exploited for better taste and longer shelf-life.  Third, we identified the causal variants for the pink tomato, which can be used for selective breeding. Pink tomato is a favorite in North China and I prefer it too, as it tastes better than the red ones. Finally, we found there have been costs to historical selection. For example, the near fixation of 25% of the tomato genome due genetic hitchhiking that occurred during domestication and improvement sweeps, as well as the linkage drags associated with wild introgression.

Cover of Nature, May 2012

Were you at all surprised to find such a large number of domestication and improvement sweeps? Did these results differ at all from other prominent vegetables, such as cucumber or potato?

The number and genomic proportion of domestication sweeps in tomato are similar to those in cucumber. However, the linkage disequilibrium blocks are bigger in tomato than in cucumber, possible due to the fact that tomato is a self-crossing species. Based on our data, we predict that the effective population size of tomato at domestication was about 300, similar to that of cucumber (~500), which is significantly smaller than that of maize (~150,000). This means these two vegetables have undergone much more severe bottlenecks during domestication as compared to maize.

How do you envision tomato breeders using the results of your study?

As a result of this work, tomato breeders will have a panoramic view of tomato variation and a better understanding of the raw materials used in their own breeding programs. From a practical standpoint, they will have access to a database of 11 million SNPs, from which they can pick the ones best suited to their molecular breeding programs. For example, they can combine the SNP dataset with their phenotypic data, to elucidate the genetic bases of important traits. Finally, and importantly I think, they will better understand the limitations of conventional breeding and the cost of historical selection, which will give them clues to improve their future programs.

NRCSHI07018_-_Hawaii_(716072)(NRCS_Photo_Gallery)

{credit}Photo courtesy of USDA Natural Resources Conservation Service{/credit}

Congratulations on your recent move to the Agricultural Genome Institute at Shenzhen where you are a co-founding director. Can you tell us a little about this new institute and what its goals are?

Thanks! The leadership of the Chinese Academy of Agricultural Sciences set up the institute (AGIS) to innovate agricultural research using genomics.

AGIS is located at the Dapeng District of Shenzhen, a beautiful bay area. The Shenzhen municipal government is developing the Dapeng Peninsula as the International Bio-valley and high-tech agriculture is one of the highlights. AGIS will recruit ~200 scientists who will decode, analyze, and utilize agricultural genomes. There will be three themes of research: the first theme is to develop basic algorithms and bioinformatic tools tailored for agricultural genomes, many of which are quite different from the human genome that has been the focus for most bioinformatians; the second theme is to empower agricultural breeding with genomics, to increase the efficiency and effectiveness of breeding that is essential to global food security; and the third theme is to provide genomic surveillance of food safety and agricultural environment, which is a huge concern of society and a need for sustainable development.

A vegetable market in Shanghai, China

A vegetable market in Shanghai, China{credit}nadja robot via Flickr.com{/credit}

Bonus question: What is your favorite vegetable?

China is a country of vegetables, as there are over 200 kinds of vegetables that are regularly consumed in the country. I enjoy the diversity. For fruit vegetables I like tomato, cucumber, and chili; for leaf vegetables, I like Chinese cabbage, lettuce, and coriander.

 

You can read more about this exciting study at The Scientist. Read the full paper here