Where have all the crop phenotypes gone?

Perspective Where Have All the Crop Phenotypes Gone? Dani Zamir* Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel Summary: In crop genetics and breeding research, phenotypic data are collected for each plant genotype, often in multiple locations and field conditions, in search of the genomic regions that confer improved traits. But what is happening to all of these phenotypic data? Currently, virtually none of the data generated from the hundreds of phenotypic studies conducted each year are being made publically available as raw data; thus there is little we can learn from past experience when making decisions about how to breed better crops for the future. This ongoing loss of phenotypic information, particularly about crop productivity, must be stopped if we are to meet the considerable challenge of increasing food production sufficiently to meet the needs of a growing world population. Here I present a road map for developing and implementing an information network to share data on crop plant phenotypes. The Virtue of Plant Phenotypes The beauty of life is manifested in phenotypes, the observable characteristics and traits that are produced by an organism’s genetic makeup—its so-called genotype. Some phenotypes are caused by single genes, others by multiple genes that can generate different phenotypic outcomes depending on how they interact with each other and with the environment. Phenomics—the systematic study of phenotypes on a genome-wide scale—generates data that are orders of magnitudes more complex to obtain and archive than the four-base nucleic acid code or the twenty amino acids that make up proteins. Unlike the publicly accessible and curated repositories built for the deposition of DNA and protein sequence data, there exists no equivalent public repository for the deposition of raw data generated from the hundreds of plant phenotypic studies conducted each year. This means that data that sometimes costs very large sums of money to generate is lost forever. This lack of phenotype ‘‘warehousing,’’ particularly for crop productivity phenotypes, must be stopped if we are to meet the challenge of increasing food production by 70–100% to feed the 9 billion people estimated to populate the earth by 2050 [1]. improve the phenotype. Thus it seems incomprehensible that we let such crop genetic studies be published without the deposition of the raw data in appropriate and publicly accessible databases. To give some idea of the scale of the problem, I recently searched the Web of Knowledge ISI database and found over 5,000 publications that report on QTL mapping; for less than 1% of these papers, the raw data is publicly available. Crop Genetics and the Search for Improved Plant Traits Why Bother to Share Crop Phenotypes? Plant breeding is the art and science of improving traits that are of agricultural importance, such as disease resistance or the ability to produce high yields when grown in particular environmental conditions, such as drought (Figure 1). Today, the use of thousands of genetic markers to identify the chromosomal regions that are associated with valuable traits increases the speed with which traits can be discovered, verified, and combined in breeding programs [2,3]. Crop geneticists have analysed over the past decades numerous segregating plant populations in which genomic regions, called quantitative trait loci (QTL; see Glossary, Box 1), exist that are associated with agricultural yield. More recently, genome-wide association studies (GWAS) and genomic selection experimental schemes have enriched the repertoire of breeding methods that can be used for finding improved plant traits. Phenotyping for yield and its components, whichever population structure is being used, is a rate-limiting activity of the breeding process since it requires the testing of the genotypes in different years and field environments in order to identify those QTL that more consistently An analysis of global crop production based on statistics from the United Nation’s Food and Agriculture Organization (FAO) shows that crop yields increased by 56% between 1965 and 1985, compared to only 28% from 1985 to 2005 [4]. This initial and significant increase in global crop production was achieved because of the ‘‘Green Revolution,’’ in which scientific methods and the use of pesticides, fertilizers, irrigation, mechanization, and soil conservation were successfully applied to the breeding of high-yield varieties of grain crops. A new ‘‘revolution’’ is similarly needed today to increase and accelerate crop yields. Taking the public sharing of genomic data as an example of the whole being more than its parts, I propose that the more phenotypic data we share, the faster we will achieve crop yield improvements. Making historic phenotypic data publicly available would allow plant researchers to share results, to compare their phenotypes, and to analyse those that have been deposited in the past in order to identify new, and sometimes rare, alleles that improve productivity. For example, although more than a hundred studies have been conducted in Citation: Zamir D (2013) Where Have All the Crop Phenotypes Gone? PLoS Biol 11(6): e1001595. doi:10.1371/ journal.pbio.1001595 Published June 25, 2013 Copyright: ß 2013 Dani Zamir. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funded by the European Research Council (ERC) advanced grant (Project YIELD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The Perspective section provides experts with a forum to comment on topical or controversial issues of broad interest. Competing Interests: The author declares competing financial interests as he is a co-founder of the company Phenom Networks that develops phenotype bioinformatics tools. * E-mail: PLOS Biology | www.plosbiology.org 1 June 2013 | Volume 11 | Issue 6 | e1001595 Box 1. Glossary Yield stability: how stable the yield of plant variety is over time and in different cultivation environments. Quantitative trait: a trait that is influenced by multiple genes and the environment. DNA marker: a DNA sequence with a known chromosomal location that can be used to identify traits in individuals or populations. Quantitative trait loci (QTL): chromosomal segments that are closely linked to the genes that underlie quantitative traits. Introgression lines (ILs): nearly isogenic lines, each containing a single genetically defined chromosomal segment derived from a different breed, strain, or species. Genome-wide association study (GWAS): an experimental and statistical approach in which numerous genome-wide DNA markers are assayed in different individuals to identify those that are assoc (...truncated)