Voss-Fels et al.

BMC Biology (2019) 17:18

https://doi.org/10.1186/s12915-019-0638-4

QUESTION AND ANSWER Open Access

Q&A: modern crop breeding for future food

security
Kai P. Voss-Fels1, Andreas Stahl2 and Lee T. Hickey1*

200 species are regularly consumed, and only three of

Abstract
them—rice, maize and wheat—provide 60% of the en-
Farmers around the world have recently experienced ergy in the human diet. In addition to cereals, other
significant crop losses due to severe heat and drought. major food crops include roots and tubers, sugars,
Such extreme weather events and the need to feed a pulses, nuts, oil-bearing crops, vegetables, fruits, spices,
rapidly growing population have raised concerns for and others such as tea and coffee. While food crops are
global food security. While plant breeding has been grown and harvested for profit in many developed coun-
very successful and has delivered today’s highly tries, they make an important contribution to food se-
productive crop varieties, the rate of genetic curity through global trade. In developing countries,
improvement must double to meet the projected subsistence farmers often grow food crops where hunger
future demands. Here we discuss basic principles is still a serious issue. Many crops important for local di-
and features of crop breeding and how modern ets in developing countries have received little invest-
technologies could efficiently be explored to boost ment, known as orphan crops (e.g. sorghum, finger
crop improvement in the face of increasingly millet and cassava), and with some rapid genetic im-
challenging production conditions. provement they could be cultivated more broadly to help
diversify human diets and improve farming systems
through better crop rotations.
What is the demand for plant-based food
products?
The current number of 7.6 billion people on this planet How did our major food crops evolve?
is estimated to increase to about 10 billion by 2050. The beginning of crop development dates far back into
With this rapid population growth the world has be- human history and is widely accepted to have its origin in
come increasingly urbanized and the ratio of food pro- the ‘Fertile Crescent’, a region that today spans part of the
ducers to food consumers has significantly declined. countries of Iraq, Palestine, Syria, Lebanon, Cyprus,
This has placed pressure on food production globally, Jordan, Israel, Egypt, Turkey and Iran. Recently, new evi-
but intensified, more efficient agricultural production dence emerged that prehistoric bread-like products were
has met these demands. There are, however, serious con- produced in South-west Asia 14,400 years ago [1], which
cerns that the forecasted increase in demand for were made from root tubers (Bolboschoenus glaucus) and
plant-based products by up to 70% within the next three seeds of wild einkorn (Triticum boeoticum), one of the an-
to four decades cannot be met through increased pro- cestors of today’s wheat. Interestingly, this pushes back
duction using current crop varieties and farming prac- the evidence of bread to at least 4000 years before agricul-
tices. This represents an unprecedented challenge for all ture emerged. This suggests that early bread-making cul-
related fields of agricultural and environmental research. ture may have fuelled domestication of our first crops [1].
During settlement and the advent of agriculture, humans
selected the most favourable plants of the available ances-
Which crops do we eat?
tral types, and this process of co-evolution between plant
Although about 300,000 plant species are edible, only a
species and humankind resulted in today’s food crops.
fraction of them are used for human nutrition. Around
Seeds from the best performing plants were retained after
* Correspondence: [email protected] harvest and sowed in the next season, leading to a con-
1
Queensland Alliance for Agriculture and Food Innovation, The University of tinuous improvement of characteristics favourable for hu-
Queensland, St Lucia, QLD 4072, Australia
Full list of author information is available at the end of the article
man nutrition and local production. This first form of

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
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Voss-Fels et al. BMC Biology (2019) 17:18 Page 2 of 7

breeding selection without any enforced crossing repre- as enrich human diets with more nutritious foods. Since
sented the main form of plant improvement for several the Green Revolution, steady increases in crop product-
thousands of years, shifting plant characteristics to in- ivity have occurred; however, there is concern that yield
crease their usefulness [2]. So-called domestication traits improvement is beginning to plateau. The current rate
were the prerequisite for successful cultivation. A good ex- of annual yield improvement for major crops ranges be-
ample was the elimination of the seed dispersal mechan- tween 0.8 and 1.2%, which must be doubled in order to
ism in cereals like wheat and barley, known as seed meet the highly increased future demand for plant-based
shattering. While seed shattering at maturation is essential products [3]. Without new approaches that help boost
for wild grasses to disperse and reproduce, this character- productivity of staple crops through genetic improve-
istic is undesirable for farming. Therefore, plant genotypes ment, global food security will be severely compromised
that retained their seeds and thereby showed reduced yield in the next two to three decades, given the current glo-
losses were selected in the process of domestication. Be- bal consumer behaviour. There are two main avenues by
cause only few plants carried the desirable mutations, the which crop productivity on farms can be improved: i)
strong selection pressure acted as a genetic bottleneck on through the deployment of genetically superior crop var-
the diversity available in our modern crops (Fig. 1a). Con- ieties, or ii) via the adoption of better management prac-
sidering the extremely long evolution of crops, modern tices. Ideally, both are addressed in parallel to provide a
plant breeding has only recently been practiced, mainly step-change in productivity, similar to what was
after the formulation of Mendel’s Laws of Heredity in achieved during the Green Revolution (see below). One
1865. Mendel’s early genetic studies on peas and his of the major bottlenecks of plant breeding is the time it
resulting theories about inheritance and trait segregation takes to develop an improved crop variety. Traditionally,
paved the way for targeted crossing between parental ge- it can take one or two decades because of the many
notypes, a practice that underpins modern crop improve- steps of crossing, selection and testing required. There-
ment. However, in order to be able to meet the increasing fore, plant breeders and researchers around the world
demand for plant-based products, rates of genetic im- are developing new technologies and approaches to help
provement must be doubled by the middle of this century. speed up the efficiency of crop breeding. On farms, the
adoption of poor or suboptimal management practices
Why the need for speed? results in a yield ‘gap’, where the potential of crop yields
New technology and advances in science offer new op- are not realised. This gap exists even in developed coun-
portunities to further improve the efficiency of agricul- tries, but is often largest in developing countries where
ture while reducing its environmental footprint, as well machinery and other equipment and supplies, along with

Fig. 1. Development of crops over time, including a the loss of the diversity through the genetic bottlenecks of domestication, selection of
landraces and modern plant breeding (adapted from [10], with permission from AAAS), and b example of a tall wheat landrace grown prior to
the Green Revolution (left) and a modern high yielding cultivar selected for reduced plant height (right)
Voss-Fels et al. BMC Biology (2019) 17:18 Page 3 of 7

agronomy advice, are not readily available. Closing the also play a key role in determining the plants’ perform-
yield gap is considered a challenging, yet high-priority, ance in a given environment.
goal for enhancing productivity and global food security.
How does plant breeding work?
The plant kingdom is extremely complex and the opti-
What determines crop yield? mal plant breeding strategy is highly species-dependant.
One of the most important traits that plant breeders aim However, any breeding program can be broadly classed
to improve is ‘yield’. Depending on the species this can into three main processes: i) the creation of new genetic
be ‘grain yield’, ‘total biomass’ or ‘total amount of sugar’ variation, ii) the selection of candidates based on defined
per area harvested. Yield represents a highly quantitative merits and iii) the testing, propagation and release of im-
trait, which means that it is determined by numerous proved crop varieties. The conventional way of creating
factors, including the interplay of many underlying genes new genetic variation is to make targeted crosses be-
with typically small effects (G), the environmental condi- tween selected individuals to create progeny that segre-
tions under which the plants are grown (E) and the gate for the trait of interest, typically representing the
management practices applied (M). In most circum- start of a breeding program. After that, a main task of
stances, there is a strong interaction among the G, E and the breeder is to identify genetically superior individuals
M, which results in a high degree of complexity at the from typically large populations (thousands to tens of
level of trait expression [4]. Each of those main com- thousands of genotypes). This typically involves
plexes unfolds into several components that themselves multi-year and -location testing of candidates in repli-
represent complexes as well. In cereals, for example, the cated experimental field trials in order to estimate the
G component for grain yield can be understood as a genetic potential of a genotype across a range of growing
higher-level complex consisting of several genetically de- conditions as accurately as possible. It is important to
termined components that jointly affect yield. For a crop consider that most important crop species can be propa-
like wheat, important yield components include the gated as inbred lines or clones, thereby allowing re-
number and size of kernels per ear (e.g. per spike or peated testing of the same genotype in different
panicle) and the number of ear-producing tillers per production conditions. For most important crop species,
plant. Each of those major yield components unfolds modern selection strategies have been developed that in-
into several lower-level physiological components, for corporate genome information based on next-generation
example the number of spikelets per spike and the num- DNA sequencing technologies in the breeding process
ber of kernels that are produced per spikelet. The gen- (see below). In the final stage, breeders will typically
etic constitution of a variety directly determines its yield register their most promising variety candidates (typic-
potential, e.g. when considering genetic resistances ally only one or two) at a legal variety testing depart-
against plant diseases caused by fungal or bacterial path- ment that runs multi-year and -location evaluation trials
ogens. Major environmental effects that are relevant to to assess if the variety has distinctly improved character-
plant breeding are the amount of water that is available istics that warrant its official registration. Once regis-
for the plant (mostly determined by frequency and dis- tered, the new variety becomes available to farmers.
tribution of precipitation), soil composition, radiation in- Depending on the crop this process can take up to one
tensity and temperature. Interactions of G and E are to two decades, making breeding programs very rigid
most extreme when the order of merit of different var- and complex endeavours.
ieties changes depending on the environmental condi-
tions they were grown in. For example, a maize variety How does the mode of reproduction determine
that produces a very shallow root system and allocates the breeding strategy?
relatively limited resources to below-ground plant devel- The main principle ways of sexual propagation relevant to
opment might be able to produce significantly higher most crop species are outcrossing and inbreeding [4]. Out-
yields than a variety that produces a large, deep-reaching crossing species sexually reproduce through hybridization
root system when both varieties are grown at a location of gametes from two different plants, whereas for inbreed-
characterised by sandy soils with a low water storage ing species both gametes originate from the same plant.
capacity and frequent rainfalls throughout the growing Many important cereal crops, such as wheat and barley, are
season. However, the situation changes entirely when inbred species that produce hermaphrodite flowers. These
both varieties are grown on production sites that are flowers have biological mechanisms that minimise out-
characterised by deep soils with a high water storage crossing. Classical breeding strategies that have been widely
capacity and extremely low precipitation throughout the used for these crops are referred to as ‘pedigree breeding’
crop-growing season, leading to severe droughts. Espe- approaches, typically resulting in fully homozygous line var-
cially phenology-related traits like flowering time can ieties. Here, plant breeders make crosses by manually
Voss-Fels et al. BMC Biology (2019) 17:18 Page 4 of 7

removing anthers from the ‘female’ plant (known as emas- producers, researchers and other breeders, although
culation) and then apply pollen from a different ‘male’ there are IP regulations and material transfer agreements
plant. In this way, directed crosses can be made even for in- involved. On the other hand, seeds produced by private
breeding species. Depending on the size of the breeding plant breeding programs underlie stricter IP regulations
program the total number of directed crosses can range be- and have to be purchased through the breeding com-
tween less than 100 to a few thousand. The offspring segre- pany or the contracted seed distributor. Several inter-
gate and breeders select the best plants during multiple national research institutions run public crop breeding
rounds of recurrent inbreeding and field testing. A high programs. For example, CGIAR represents a very large
level of homozygosity is critical to ensure that the variety global partnership consisting of 15 agricultural research
that is grown by farmers does not segregate further, poten- organisations whose joint agenda aims at improving glo-
tially exposing recessive genetic variants with detrimental bal future food security, reducing poverty and improving
effects on agronomically important traits. In outcrossing human health and nutrition. Their joint investments into
species, breeders aim to improve a plant population from crop improvement run into the billions of US dollars.
which the best individuals are recurrently selected and One of the partners is CIMMYT (The International
intercrossed during the breeding program, making it con- Maize and Wheat Improvement Centre) based in
ceptually different from line breeding for inbreds, which re- Mexico, which is leading the wheat and maize improve-
sults in one single, improved genetically homozygous line. ment programs. CIMMYT has developed numerous var-
The rate of success of population breeding programs de- ieties grown on millions of hectares worldwide. Another
pends on whether the target traits are expressed before or important public crop improvement organisation, which
after flowering, determining how efficiently unfavourable is heavily involved in the improvement of rice varieties,
individuals can be removed to ensure that they are not is the International Rice Research Institution (IRRI)
passing on genetic material to the next generation. One of based in the Philippines, representing the largest
the most popular strategies for outcrossing crop species is non-profit agricultural research organisation in Asia.
hybrid breeding. Here, two genetically distant inbred lines Public crop improvement programs are also important
are crossed to generate fully uniform F1 hybrids that show for ‘pre-breeding’, which bridges discovery research and
a significantly higher performance than both parents. This applied crop breeding. On the other hand is the private
approach takes advantage of a phenomenon called heterosis plant breeding sector, which is dominated by big multi-
(or hybrid vigour) and while different theories have been national companies like Bayer, Syngenta and Corteva.
developed, its biological basis remains elusive. In maize, These companies produce and commercialise seeds of
spectacular yield increases have been realised since the im- highly productive varieties that can be purchased by
plementation of hybrid breeding in the early twentieth cen- farmers. In Europe, for example, there is a strong
tury. In rice there are hybrids that produce up to 30% more mid-tier for plant breeding consisting of small to
yield than common inbred lines. However, a major chal- mid-scale companies. While the big players mostly con-
lenge is to practically ensure directed crossing and efficient duct breeding research using their own facilities and
production of hybrid seed. Breeders typically deploy genetic in-house resources, smaller companies typically depend
sterility mechanisms to make sure that genotype A is only on collaborative R&D activity with public research insti-
pollinated with pollen from genotype B without pollen con- tutions and/or other small companies.
tamination from other sources (e.g. other genotypes or
self-pollination), although chemical hybridization agents What was the green revolution?
that are typically less efficient are used for some species. The Green Revolution describes the tremendous in-
This restricts the availability of hybrid varieties for some crease of grain yield associated with improved genetics
crops, like wheat and barley. For commercial breeders hy- and application of plant protection chemicals and min-
brid varieties are very attractive because farmers cannot re- eral fertilizers. While it took almost 10,000 years for
grow the seeds they harvested but have to buy new seeds in humans to produce one billion tons of grain globally,
every growing season. This is because seeds harvested from the Green Revolution led to a doubling of that amount
F1 hybrids (i.e. the F2 generation) will cause serious yield in just 40 years between 1960 and 2000. A key driver of
decreases (due to the 1:2:1 segregation), protecting IP of the Green Revolution was the introduction of so-called
the hybrid variety and promoting higher profits from seed semi-dwarfing genes (reduced height, Rht-genes) in
sales each year. wheat. Varieties carrying the Rht genes were shorter
(Fig. 1b) and much better at utilizing increased amounts
Who is breeding the crop varieties? of applied nitrogen. In comparison to taller varieties,
Crop improvement programs are run in both the public which tend to lie flat on the ground (lodging) as a result
and private sector. Public plant breeding programs typic- of high nitrogen fertilization and/or increasing grain
ally produce germplasm, which is freely available to load, Rht-carrying varieties contribute to a better
Voss-Fels et al. BMC Biology (2019) 17:18 Page 5 of 7

nitrogen use efficiency, preventing nitrogen from being temperature change will not likely lead to dramatic yield
wasted and polluting neighboring ecosystems [5]. Today, losses [7]. It is very difficult to attribute specific weather
dwarfing genes are widespread in modern cereal varieties events to climate change since effects are mainly meas-
worldwide and a range of different Rht genes have been urable as long-term trends. Furthermore, environmental
characterized. The first deployed Rht genes, including effects on crop yields can vary strongly from year to
Rht-B1b (formerly Rht1) and Rht-D1b 8b (formerly year. There are arguments that with increased tempera-
Rht2) originated from the Japanese wheat variety ‘Norin tures the atmosphere can hold more water. However,
10’, which is a progeny of the Japanese semi-dwarf land- different spatiotemporal evaporation rates which are not
race ‘Daruma’ and an American high-yielding variety. synchronized with increased atmospheric water holding
Norin 10 was central for the creation of several import- capacity drive changes in global precipitation. Hence,
ant Green Revolution wheat varieties. Also for barley drought events are predicted to become more frequent
and maize the orthologous genes sln1 and dwarf8 were and severe in many crop-growing regions. Plant breeding
discovered. These genes generally encode transcription is expected to play a central role in meeting the chal-
factors that target components of the gibberellin acid lenge to adapt crops to future growth conditions.
(GA) pathway, which regulate GA response. GA is a
tetracyclic diterpenoid acid that is important for the on- What is the genomics era of crop improvement?
set of flowering and pollen development, as well as a key Over the past ~ 10,000 years, crops were mainly im-
determinant of cell elongation and therefore plant proved through selection of superior individuals that
height. Consequently, wheat and rice plants that carry showed characteristics favourable for human nutrition
semi-dwarfing genes are shorter and realize a higher har- and production, but without enforced crossing involved.
vest index, defined as the ratio of grain yield over the en- The formulation of Mendelian laws heralded the begin-
tire plant biomass. The advent of smaller, more stable ning of modern plant breeding, which has changed tre-
varieties with a higher harvest index was accompanied mendously over the past 150 years. The introduction
by several positive effects, including an improved alloca- and continuous development of theoretical frameworks,
tion of nutrients and assimilates to the grains and a re- including quantitative genetics principles and the rapid
duction of residual plant biomass [5]. advances in the field of modern biotechnology and gen-
omics, have made plant breeding a very complex discip-
How does climate change affect crop production? line [2]. Modern plant breeding programs involve expert
Climate change is a generic term that describes the re- teams that combine very broad and different skillsets,
cent and forecasted change of multiple environmental such as genetics, statistics, agronomy, biochemistry,
parameters. Most of them, including atmospheric CO2 physiology, bioinformatics, molecular biology and eco-
concentration, temperature and the frequency and nomics, making them highly interdisciplinary. Advances
amount of precipitation, affect plant growth. While a in DNA sequencing technologies have revolutionised
higher CO2 concentration usually increases photosyn- crop breeding and research, opening up the ‘genomics
thesis, a lack of rainfall at critical developmental stages era’ of crop improvement. Today, whole-genome refer-
decreases crop yields. The record-breaking Millennium ence DNA sequences are available for most important
droughts in 1996/97, 2001–2003, 2006 and 2018 in crop species and very cost-efficient genotyping platforms
Australia or 2003, 2010, 2015 and 2018 in Europe are to ‘DNA fingerprint’ plants have been developed. The
examples for extreme effects of drought on crop produc- DNA marker of choice is typically
tion. On the other hand, like CO2 concentration, in- single-nucleotide-polymorphism (SNP) markers because
creasing temperature can accelerate plant growth due to they are ubiquitous in crop genomes and very easy and
a higher enzymatic activity. Beyond the temperature cost-efficient to score. It has therefore become standard
optimum, which is very crop and variety specific, higher practice in modern crop improvement to genotype large
temperatures result in heat stress, which is considered a populations of plants with thousands to tens of thou-
major cause of wheat yield loss in developing countries. sands of markers on a routine basis. Even whole-genome
It has been estimated that each °C increase leads to a de- resequencing data are becoming increasingly available,
crease of global wheat production of 6% [6]. Increasing providing unprecedented insights into structural diver-
temperature can also indirectly affect crop yields due to sity across crop genomes [8]. Using the latest statistical
an increased occurrence of pests and diseases. Clearly, genetics approaches, vast amounts of genotype data are
the magnitude of impact of climate change on crop used for various purposes. For instance, a very promising
yields will depend on the geographic region. For ex- modern selection strategy that incorporates
ample, an increase in temperature of 4 °C has been fore- genome-wide DNA marker information is ‘genomic se-
casted to reduce wheat yields by 20–30% in tropical lection’ in which statistical models or machine learning
regions, whereas in temperate regions, the same algorithms are deployed to link genomic polymorphisms
Voss-Fels et al. BMC Biology (2019) 17:18 Page 6 of 7

to phenotypic variation. The underlying theoretical introduced should be considered a non-GM tool. Alter-
foundation of the approach is that genes (or more gen- natively, ‘speed breeding’ developed by Dr. Lee Hickey
eric quantitative trait loci (QTL)) that affect the trait of and colleagues provides a non-GM route to rapidly
interest (e.g. grain yield) are tagged by DNA markers, introduce or stack new trait variation. This technique
allowing one to derive effect approximations for each of uses controlled environmental conditions and extended
those QTL on the target trait. A prediction equation is photoperiods to achieve up to six generations per year,
used to calculate a genomic estimated breeding value for instead of just one or two in the field. This can speed up
each genotype, based on whole-genome marker profiles, the development of inbred lines following a cross, simi-
without actually testing those genotypes in field trials. lar to doubled haploid technology, which is a lab-based
This allows breeders to predict genotype performance as technique that has been a revelation for breeding crops
soon as DNA marker profiles can be generated (i.e. at like maize and winter wheat. Most of the modern tech-
seedling stage). Ultimately, the time until selection deci- nologies have been proven to assist the development of
sions are being made is significantly decreased, which improved crop varieties. However, more efficient breed-
leads to increased genetic gain per unit of time. Since its ing strategies that effectively combine these technologies
formal introduction in 2001, genomic selection has led could lead to a step-change in the rate of genetic gain.
to tremendous increases in genetic gain in animal breed- Ongoing investment from the public and private sectors
ing (e.g. dairy cattle) and it has a huge potential for crop is necessary to build and maintain capacity for sustained
improvement as well. crop improvement to ensure the development of crops
that are capable of feeding the world in the future.
Can new technologies speed up crop
Acknowledgements
improvement? LTH was supported by an Australian Research Council Early Career Discovery
The rate of improvement of genetic yield potential has Research Award (DE170101296). LTH and KPV-F give thanks to the re-
to be increased beyond the rates currently achieved in searchers at the James Hutton Institute and the University of Dundee for
fruitful discussions on crop breeding topics during their visit to Scotland
ongoing breeding programs to protect global food secur- through the UUKI Rutherford Fellowship program. AS is grateful for a travel
ity in times of rapid population growth and climate scholarship provided by the German Academic Exchange Service (DAAD).
change. Thus, new or different approaches are needed to
accelerate the crop breeding process. Over the past de- Authors’ contributions
The authors jointly conceived the article, conducted the literature review and
cades, numerous technologies have emerged that can ac- wrote the manuscript. All authors read and approved the final manuscript.
celerate plant breeding, such as genomic selection
(described above). In addition to genomics approaches Competing interests
described above, other new methodologies such as gene All authors declare that they have no competing interest.

editing technology are fast-evolving and protocols have

been refined for most major crop species. In CRISPR Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in
gene editing systems, guide RNA directs the Cas9 en- published maps and institutional affiliations.
zyme to the target DNA site and cuts the DNA. This
can be used to activate or deactivate alleles of a target Author details
1
Queensland Alliance for Agriculture and Food Innovation, The University of
gene to enhance plant performance, e.g. through im- Queensland, St Lucia, QLD 4072, Australia. 2Department of Plant Breeding,
proving disease resistance or drought tolerance [9]. Des- IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig
pite the promise of gene editing and strong support University, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany.
from the scientific literature regarding safety and sus-
tainability, many countries have employed strict legal
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