REVIEWS

Cite as: Y. Eshed and Z. B. Lippmann,

Science 10.1126/science.aax0025 (2019).

Revolutions in agriculture chart a course for targeted

breeding of old and new crops
Yuval Eshed1* and Zachary B. Lippman2,3*
1
Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel. 2Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, NY, USA.
3
Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, NY, USA.
*Corresponding author. Email: yuval.eshed@weizmann.ac.il (Y.E.); lippman@cshl.edu (Z.B.L.)

The dominance of the major crops that feed humans and their livestock arose from agricultural
revolutions that increased productivity and adapted plants to large-scale farming practices. Two hormone
systems that universally control flowering and plant architecture, florigen and gibberellin, were the source
of multiple revolutions that modified reproductive transitions and proportional growth among plant parts.

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While step-changes based on serendipitous mutations in these hormone systems laid the foundation,
genetic and agronomic tuning was required for broad agricultural benefits. We propose that generating
targeted genetic variation in core components of both systems would elicit a wider range of phenotypic
variation. Incorporating this enhanced diversity into breeding programs of conventional and underutilized
crops can help meet future needs of the human diet and promote sustainable agriculture.

Tens of thousands of plants have edible fruits, seeds, or other
plant parts (1). Yet, only several hundred plants are cultivated
worldwide, and humans rely on a few dozen species for the
majority of their food (1–3). This bottleneck in crop diversity
reflects the early domination of the human diet by a few pio-
neering crops that feed the masses through large-scale agri-
culture. Dramatic phenotypic changes in these selected crops,
which we define as agricultural revolutions, accelerated their
ascent over other edible plants. We discuss in this review the
changes in plant growth, physiology, and productivity that
have been and continue to be repeatedly exploited in agricul-
ture. The genetic systems underlying these changes are sum-
marized in Fig. 1, along with their universal core molecular
components. Alongside its central role in plant adaptation
(4), the universal florigen hormone system governing the
transition to reproductive growth (flowering) was repeatedly
modified during domestication and subsequent crop im-
provement. Modifications to flowering genes shifted the pro-
portion of vegetative growth (shoots and leaves) to
reproductive growth (flowers, fruits, seeds) and provided a
range of variation for shoot architecture, plant size, and
flower, fruit and seed production. Selection of specific muta-
tions adapted crops to the environmental and agricultural
conditions of high-density planting and machine harvesting.
Green Revolution “dwarfing” gene mutations that modified
the gibberellic acid (GA) hormone system prevented wheat
and rice plants from collapsing (lodging) by reducing plant
height (stature) under high productivity in chemically ferti-
lized fields, thereby minimizing yield loss due to the ill-timed
hailstorm (5, 6). The introduction of hybrid seeds a century
ago supported rapid breeding of more vigorous and fertile
maize and rice plants and simplified the stacking of disease
resistance genes in other crops such as tomato (7, 8). Genetics
changes that prevented yield loss from shattering of pods and
seeds (9) were also revolutionary, but regulation of this trait
has not been integrated into a coherent genetic path that can
be extrapolated and exploited for diverse crops. Here, we fo-
cus on the main features that unite the successful adaptations
of plants to modern agriculture, and the ongoing process of
crop improvement. We discuss how our current understand-
ing and manipulation of the underlying genetic and molecu-
lar mechanisms behind revolutions involving the florigen
and GA hormone systems can help improve major crops and
also bring underutilized crops into mainstream agriculture.
Flowering and reproductive cycling are key for field per-
formance
Florigen is the plant hormone that universally translates en-
vironmental cues and endogenous signals to initiate flower-
ing (10). Unlike other plant hormones, florigen is a globular
protein produced in leaves and delivered systemically to api-
cal and axillary tips of shoots (buds) (11, 12). The flower-pro-
moting activity of florigen is counteracted by products of
genes from the same family that encode antiflorigenic hor-
mone signals, (13). Together, the opposing hormones com-
prise a tunable and environmentally timed regulatory system
that directs both systemic and local cues toward flowering.
This balanced hormonal relationship is critical for flowering
plants to navigate between two opposing needs – the produc-
tion of sufficient vegetative shoots and leaves (source tissues)
to support the high metabolic demands of developing flow-
ers, fruits and seeds (sink tissues), but also the timely

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completion of growth and seed production before growing
seasons end.
While this generic description of the florigen-antiflorigen
relationship fails to capture the dynamic evolution of the flo-
rigen gene family and species-specific mechanistic interplays
between its members (14), it allows a generalization of their
impact on plant architecture and reproductive success (Fig.
1). Particularly relevant to agriculture, and the foundation of
this review, are the many plants for which the transition to
reproductive growth is followed by repeated cycles of vegeta-
tive and reproductive growth to generate vines or bushes that
bear flowers and fruits within a growing season (15). Reitera-
tive flowering is initiated when florigen levels are high
enough to stimulate flowering in the main apical bud,
whereas newly formed vegetative buds are transiently inhib-
ited from flowering by local production of antiflorigenic sig-
nals. Production of such florigen counterbalancing signals is
typical of many short-lived perennials and represented by
crops like soybean and tomato (16).
The first description of a balance between positive and
negative flowering signals emerged from grafting studies in
the 1970s on the tomato relative tobacco by Mikhail Cha-
ïlakhyan and Anton Lang (17). Two decades later, the first an-
tiflorigen molecule was discovered by studying the tomato
self pruning (sp) mutant (18). A rare natural variant discov-
ered in a farmer’s field in the 1920s, sp, catapulted tomato
into large-scale open field production, transforming the agri-
cultural landscape of California’s Central Valley (Fig. 2) (19).
Aptly named, sp effectively “annualized” tomato by convert-
ing the endless cycling between vegetative and reproductive
growth into a new plant form where successive side shoots
flower more rapidly than the one before until new growth
eventually ceases (18). In broad terms, the loss of antiflorigen
signals removed inhibition of florigen activity in newly devel-
oping side shoot buds. The result was a novel compact shoot
system with a burst of flowering and fruit production that
was immediately recognized for its potential agronomic value
(19, 20).
Mutations in antiflorigen genes underlie a common syn-
drome in domestication and crop improvement that revolu-
tionized agriculture. The crop list includes multiple legumes,
including soybean, and extends to strawberries, sunflower,
and non-food plants, such as rose and cotton (Fig. 2) (21–23).
Although phenotypic consequences and benefits from anti-
florigen mutations can manifest in species-specific ways,
such as shorter, more compact soybean plants with reduced
lodging and continuous fruiting in strawberry (21, 24, 25), the
unifying physiological change is an acceleration of matura-
tion, often associated with precocious flowering of side
shoots that converts continuously growing (indeterminate)
shoot systems into compact (determinate) plants with con-
centrated flowering, fruit set and ripening in both time and
First release: 5 September 2019 www.sciencemag.org
space. For major crops like tomato and soybean, this propor-
tional shift to more reproductive growth provided faster
growing cycles that allowed adaptation to shorter growing
seasons or multiple plantings in longer seasons, and also per-
mitted higher planting densities to increase yield and pro-
mote innovation in mechanical harvesting. While this
agricultural revolution occurred within the last century for
tomato (19), it emerged multiple times during soybean do-
mestication over 5000 years ago (24, 25). Despite these differ-
ent time scales, and like the many other crops that benefitted
from both subtle and sudden step changes in flowering and
plant architecture from mutations in antiflorigen or florigen
genes (26–37), these few fortuitous alleles alone could not
provide broad environmental and agronomic adaptations.
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Tuning as the basis of agricultural revolutions
Ancestral relatives of modern crop plants originated from di-
verse environments and geographical ranges and evolved un-
der selection pressures for ecological success. Adaptation of
such plants for agricultural use demanded modifications of
the wild ancestral forms (38). In several cases, rare mutations
resulted in trait and species-specific qualitative changes of
immediate benefit. However, for obtaining tuned maturation
from antiflorigen mutations, additional adjustments were re-
quired to modify vegetative to reproductive growth balances
and to develop different varieties with maximized productiv-
ity under the specific conditions of modern agriculture. For
example, selection for slightly earlier or later flowering in
soybean and tomato antiflorigen mutant backgrounds pro-
vided varying levels of determinacy that influenced both ad-
aptation and yield for different lengths of growing seasons
(39–41). Such quantitative changes were achievable because
of the inherent tunability of the florigen-antiflorigen system.
Analogous to the tuning of florigen-antiflorigen is the reg-
ulation of plant height, or stature, by the GA hormone system
(Fig. 1) (42). Synthesized through a complex multistep path-
way, active GA is sensed by intracellular receptors Gibberellin
Insensitive Dwarf 1 (GID1) that direct the destruction of a ge-
neric growth repressor protein DELLA (43). GA is also not
essential for the formation of particular organs or cells and
thus is another system primed for quantitative tuning. GA by
itself regulates flowering in many plants, including cereal
crops (44). Thus, the two hormone systems, through inde-
pendent mechanisms, translate quantitative environmental
readouts into developmental timing and growth, as opposed
to hormones with fundamental roles in cellular and tissue
identity and morphogenesis, such as auxin and cytokinin.
A modern agricultural revolution was based on genetic
modification of the GA system (Figs. 1 and 3) (5). Beginning
more than 50 years ago, introduction of gain-of-function
DELLA mutations in wheat (6, 45) and later loss-of-function
mutations in GA biosynthesis genes in rice (46) created
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shorter, more compact plants, providing a specific agronomic
adaptation to field conditions that are chemically fertilized.
In both cases, breeders recognized the potential of these
“dwarfing genes” to overcome lodging, a drawback of unre-
stricted growth due to fertilization in which the plants col-
lapse and harvest is lost. Like tomato sp, these mutations
were insufficient on their own. First attempts to achieve de-
sired outcomes failed, and intensive and directed breeding
programs were needed to quantitatively tune the qualitative
effects of different dwarfing alleles into elite germplasm that
contained the diversity and modifier mutations to optimize
the initial dramatic change (47). Ultimately, several alleles
and selections around those alleles over several decades were
needed before the first properly tuned cultivars were released
(Fig. 3) (48). The result was a doubling of yields for rice and
wheat during the Green Revolution of the 1970s that helped
feed billions of people.
Major factors and numerous modifiers
Combining genetic diversity through hybridization followed
by segregation and phenotype-based selection is at the heart
of crop improvement. Such iterative breeding schemes are
designed to incrementally enhance field performance by unit-
ing many alleles scattered across the genome, with the ma-
jority having small effects. Indeed, quantitative genetics
studies in maize have found hundreds of small-effect loci that
act largely independently to regulate flowering time and
plant height (49, 50). Gaining productivity under such com-
plexity has been facilitated through genomic selection, which
uses genome-wide molecular markers to predict and select
higher performing lines for breeding (51). Genomic selection
is at the forefront of plant and animal breeding and illus-
trates the residual value of standing genetic variation (52).
However, expanding genetic variation beyond what nature
has provided presents a complementary approach with po-
tential to bring step changes in productivity. Specifically,
given that rare mutations of florigen-antiflorigen and GA-
DELLA mutations spawned multiple revolutions, it is highly
likely that creating novel diversity in these two hormone sys-
tems will further unleash agricultural benefits.
Studies in genetically tractable plants such as Arabidop-
sis, tomato, and rice indicate that all flowering pathways ul-
timately converge on the florigen-antiflorigen hormone
system (12, 13), the components of which can be divided into
core and peripheral regulators. The core regulators function
universally in all flowering plants and comprise the major
florigen (Arabidopsis FT/tomato SFT) and antiflorigen
(TFL1/SP) family members and their interacting proteins, the
FD/SPGB/SSP bZIP transcriptional regulators. Though most
species have multiple paralogs for these core components,
one or two are usually prominent in function, and other
closely related genes can be quantitative modifiers. For
First release: 5 September 2019 www.sciencemag.org
example, tomato has several antiflorigen paralogs (16), but
mutations in SP are sufficient for determinate growth and
short stature (Fig. 2). Mutations in a paralog of SP can accel-
erate flowering and enhance sp determinacy, providing early
maturing smaller plants suited for high density planting (53).
Similarly, in soybean, several ancient dt1 alleles function like
tomato sp to prevent excessive growth and lodging; most if
not all dt1 alleles show similar effects (24, 25). In contrast,
mutations in soybean “maturity genes”, which comprise sev-
eral peripheral regulators of florigen activity, have been crit-
ical for adjusting flowering time for varying lengths of
growing seasons (54). In some cases, specific combinations of
dt1 alleles with maturity genes have modified determinate
growth, allowing adaptations for specific growing seasons
(40, 55).
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Peripheral regulators that were important in agriculture,
especially those translating environmental stimuli to modu-
late levels of the core flowering regulators, are often specific
to plant families, with genus and even species-specific func-
tions. The soybean maturity gene mutations are alleles of
light receptors and circadian factors that alter flowering in
response to day-length by changing florigen expression (54).
Among these are interacting transcriptional regulators whose
beneficial alleles appear to be soybean specific (56, 57). The
situation is similar for potato where a different class of tran-
scriptional regulators was critical for its broad and rapid ge-
ographical spread (58). The CONSTANS gene that functions
upstream of florigen in Arabidopsis is yet another example;
orthologous mutations have opposing effects in distantly re-
lated plants (12, 59, 60), or distinct effects in related species
within the Solanales (61, 62). Thus, while peripheral regula-
tors of florigen-antiflorigen might be attractive targets in par-
ticular instances (63), their large number (64) and variable
influences can complicate tuning strategies compared to fo-
cusing on the smaller number of universal core regulators.
Potentially more amenable will be modifiers to improve the
grasses of the Green Revolution. Beyond direct improve-
ments to yield, which could also come from new diversity in
florigen-antiflorigen (65), strategies for enhancing lodging re-
sistance on top of the classical wheat Rht (DELLA) or rice sd1
(GA biosynthesis) alleles could use genes affecting traits
other than plant height (66).
Targeted genetic manipulations for tuned quantitative
variation
Creating targeted genetic variation by CRISPR-Cas genome
editing is a new and powerful addition to the classical exploi-
tation of existing or randomly induced genetic variation for
crop improvement (67) (Fig. 4). Various tools can create a
range of alleles with qualitative and quantitative effects by
targeting a selected gene, from deleting it entirely to generat-
ing specific alleles in functional domains or nucleotides in
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coding or cis-regulatory regions (68). Genome editing can ac-
celerate crop breeding in various ways. The most straightfor-
ward use would be to generate a defined mutation in the
genetic background needed, thereby eliminating the need to
introgress alleles, which is time-consuming and can nega-
tively impact productivity from linked deleterious alleles
(linkage drag). Likewise, introduction of male-sterile mutants
can expedite hybrid seed production by targeting one of the
many genes conferring this trait in one of the hybrid parents.
To speed up breeding programs, faster flowering from strong
antiflorigen mutations would shorten generation time (69).
Phenotypic benefits across many species could come from en-
hancing allelic diversity in the core hormonal regulators de-
scribed above. To illustrate the impact of targeted genome
editing, we first describe selected case studies where modifi-
cations of the florigen and antiflorigen genes improved
productivity.
In determinate tomato (sp mutants), heterozygous loss-of-
function mutations in florigen or interacting transcriptional
regulators weakened determinacy to produce a range of pro-
gressively larger, but still determinate, plants with higher
yields (70, 71). Likewise, hybrid vigor (heterosis) in rice was
associated in part with a dosage effect from a loss-of-function
florigen mutation (72). These rice hybrids exhibit slightly pro-
longed flowering that translates to more flower production
and grain yield, while maintaining an acceptable growth pe-
riod. That mutations in florigen or antiflorigen have effects
as heterozygotes in divergent species attests to a universal
dosage sensitivity that could be exploited with coding or ex-
pression alleles in both inbreds and hybrids. Eliciting contin-
uums for flowering, plant architecture, and yield can take
many targeted genetic paths. The protein products of the core
genes can be structurally modified to generate loss-of-func-
tion alleles of varying strengths (71, 73). Florigen activity is
determined by a conserved pocket or a small loop domain,
and altering specific amino acids can result in loss-of-func-
tion alleles or even convert a florigen to an antiflorigen (74).
A yield-enhancing tomato florigen variation is due to an
amino acid change in a loop domain; an identical allele af-
fecting flowering was recovered in an Arabidopsis study that
created dozens of other potentially agriculturally useful flori-
gen alleles (71, 74). In soybean, different dt1 lines might ben-
efit from similar weak alleles of florigen paralogs to slightly
suppress determinacy, resulting in one or two additional
flowering nodes before side shoots terminate. Alternatively, a
range of determinate growth lines could be created de novo
by generating a dt1 allelic series. A complementary approach
is creating variation in cis-regulatory regions, to decrease or
increase expression levels by deleting activator or repressor
domains, respectively (68, 75). Florigen-based rice heterosis
could be mimicked or exceeded by creating weak transcrip-
tional alleles of florigen in a homozygous state in elite inbred
First release: 5 September 2019 www.sciencemag.org
varieties.
The same principles, logic, and approaches can be ex-
tended to modifications of the GA system. Strong GA mutants
may have adverse physiological effects, such as sterility or
low nitrogen use efficiency (76). The adverse effects could be
annulled by second site modifiers or weaker alleles (77). Sup-
porting the latter, GA has long been used as a dose-controlled
hormone spray for diverse horticultural applications, as a
growth regulator for ornamental plants or to promote fruit
development in seedless grapes (78). The GA receptor, metab-
olism, and DELLA genes comprise the core of this growth
hormone system (Fig. 1). As for florigen and antiflorigen,
there are species-specific differences in gene family size and
expression patterns. For example, there are multiple DELLA
genes in soybean, but only one in tomato (79), and the reverse
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is true for GA receptors in tomato and rice (80). Such differ-
ences should be considered when prioritizing targets, espe-
cially when function is divided temporally and/or spatially
among multiple paralogs. Thus, even when focusing on the
core targets, genetic and molecular characterization of the
hormonal systems in each plant will be important for design-
ing both universal and specific modifications. Successful tun-
ing and outcomes will require creating collections of alleles
in different breeding lines or varieties, and then subjecting
this allelic diversity to phenotypic selection. Modifiers can
vary between genotypes, and the effect of a new allele will be
influenced by both additivity and epistatic interactions with
these modifiers (81). Thus, having extended genetic variation
will increase the likelihood of identifying alleles or allelic
combinations optimal for specific inbred or hybrid crop ap-
plications, in turn reducing the need for time-consuming
fine-tuning.
Expanding agricultural horizons: Feeding humans, not
their livestock
The collision course of ever-increasing human population
with a deteriorating climate pose significant challenges for
crop improvement scholars. Several paths are being pro-
posed, including increasing stress resilience, expanding agri-
culture into new environments such as urban habitats or
drought prone regions, and promoting a global dietary switch
to plant dominated nutrition. The two main strategies are im-
provement and further adaption of the major crops that al-
ready benefit from large-scale agricultural infrastructure
developed around them, and the diversification of agriculture
by developing new crops that would better fit climatic
changes and address nutritional needs.
Genome editing along with standard genetic engineering
tools may speed up both crop improvement and adoption of
new crops, with a recent focus given to the ease and simplic-
ity of implementing CRISPR genome editing for the relatively
few crops amenable to traditional transformation. Several
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studies have demonstrated the possibilities, with a few of the
most recognized examples being extended shelf life for mush-
rooms and creating disease resistance in wheat (82, 83). How-
ever, plant biology has exposed dozens if not hundreds of
beneficial gene and trait targets that could improve crops in
myriad ways. With this in mind, our focus on the florigen and
GA hormone systems is seemingly narrow, but which we ad-
vocate may yield the greatest return for crop improvement,
especially for the challenge of feeding more people off of less
land. We are optimistic that ongoing efforts to advanced ge-
nome editing tools and technologies for plant and genotype-
independent transformation will soon pay off (68).
Wheat agriculture in Canada is one example in which a
classical crop could benefit from expanded geographical
range. The major impediment is the short growth season,
which can be addressed by accelerating flowering and creat-
ing shorter stature varieties that will maintain productivity
under higher planting densities. This concept follows the suc-
cessful introduction of sp into Chinese cotton lines (Fig. 2),
which are high performing and grown further north than any
functional SP cultivars (84). Another benefit of earlier flow-
ering is evasion of early freezing temperatures at the end of
short growing seasons, or late-season drought as has already
been proposed for wheat (85). Potato, a clonally propagated,
self-incompatible tetraploid crop, would benefit greatly from
a diploid inbred breeding program. Gene editing has over-
come self-incompatibility in wild potato diploids (86), allow-
ing identification and purging of accumulated deleterious
recessive mutations (87). However, flowering adaptations
and improved tuber production will be needed, which could
come from tuning the already well-characterized florigen and
antiflorigen genes in potato (Fig. 5) (88).
Globally sustainable food production requires people to
shift from a livestock-based diet to a plant-based diet (89).
This change will require higher production of protein rich
crops for direct human consumption and may thus require a
switch from high calorie staple producers such as rice to high
protein producers such as protein rich cereals as well as ex-
panded cultivation of legumes. The rapid expansion of soy-
bean cultivation and its high productivity serves as a guide
for achieving these goals with other legumes. Many high-pro-
tein orphan legumes such as cowpea, lentil, lupin and pigeon-
pea could see immediate benefits from tuning florigen-
antiflorigen. Attractive among these is the drought resistant
chickpea that can grow in the dry Middle East or northern
states of India. Breeders of this underutilized crop have al-
ready selected for one high florigen producing haplotype (28),
but greater allelic diversity could increase opportunities for
chickpea cultivation.
In many parts of the world, so-called orphan crops are
grown in marginal lands characterized by harsh conditions.
Utilizing these crops may require combining universal and
First release: 5 September 2019 www.sciencemag.org
specific targets, as demonstrated for groundcherry, a distant
relative of tomato (90). Dozens of African orphan crops are
the focus of an international genomics-enabled breeding pro-
gram (91). Among these is teff, a drought resistant cereal with
protein-rich grains (92). Like many grasses, lodging is a com-
mon problem for teff, which is also characterized by excessive
branching and tiny seed size. Improvements could begin with
foundational mutations in Green Revolution GA genes to im-
prove lodging. Tailoring higher expression of branching
genes could reduce excessive production of lower branches
(tillering) by mimicking domestication alleles of teosinte
branched 1 (tb1) from maize (93), while larger seeds could re-
sult from recreating beneficial alleles of known grain size
genes (94, 95). Similarly, quinoa and its relative amaranth are
pseudocereal orphan crops from the Americas that carry
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large, heavy inflorescences (96, 97). Mutations in the florigen
or GA systems could be used to reduce height and support
broader geographical distribution. Here again, enhancing
other traits, such as seed size, may further improve produc-
tivity as larger seeds that are easier to capture at harvest. Pro-
spective biofuel crops may also benefit from shifting florigen-
antiflorigen balance, but in the opposite direction (Fig. 5). De-
laying flowering in switchgrass, for example, would promote
more vegetative growth, thereby increasing biomass yield
(98). At the opposite end, the perennial kiwi tree, with its vit-
amin-C rich fruit, can become year-round flowering bushes
upon SP inactivation (99). Such an accelerated maturation
may facilitate mechanical harvesting for these and other per-
ennial fruit-bearing crops, or even allow their incorporation
into vertical farming systems for urban agriculture, which are
currently limited to lettuce and related “leafy greens”. For all
these examples and many others, the ease of whole genome
and transcriptome sequencing can reveal the core florigen
and GA genes that are suggested as initial targets.
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ACKNOWLEDGMENTS
We thank D. Weiss, R. Fluhr, D. Rodriguez-Leal, U. Pedmale, A. Levi, A. Shepon, R.
Milo, and members of the Lippman and Eshed labs for comments on the
manuscript. We also thank three anonymous reviewers for constructive
comments that helped improve the manuscript. We thank J.-D. Lee, T. Zhang, J.
Ma, S. Thomas and the United Soybean Board for images. Funding: This work
was supported by the Howard Hughes Medical Institute, an Agriculture and Food
Research Initiative competitive grant from the USDA National Institute of Food
and Agriculture (no. 2016-67013-24452 to Z.B.L.), a National Science
Foundation grant (no. IOS-1556171 to Z.B.L.), the National Science Foundation
Plant Genome Research Program (grant nos. IOS-1546837 and IOS-1732253 to
Z.B.L.), ISF (grant nos. 1788/14 and 2731/16 to Y.E.), and BARD, the United
States-Israel Binational Agricultural Research and Development Fund (research
grant no. IS-5120-18C to Z.B.L. and Y.E. Competing interests: Z.B.L. is a paid
consultant for and a member of the Scientific Strategy Board of Inari Agriculture.

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climbing woody perennial with long juvenility and axillary flowering into a compact

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Fig. 1. Genetic systems underlying agricultural revolutions. Two hormone
systems are central to major agricultural revolutions that modified flowering,
shoot architecture and plant stature. The genetic and molecular mechanisms
underlying these hormone systems, florigen-antiflorgen (A) and gibberelic
acid (GA)-Della (B), have been dissected. In both systems a balance between
promoting and inhibiting signals can be modified genetically to quantitatively
tune the impacted traits. For nearly all crops, the transition to flowering was
modified through core and peripheral regulators of florigen-antiflorigen to
allow growth outside native habitats and enable large-scale field production.
These improvements include more rapid maturation, concentrated flowering
and fruit/seed production, and shorter stature. Modified balance of GA-Della
sparked the Green Revolution for wheat and rice. Shorter statures for both
crops prevented stem bending that causes plants to fall over during growth
(lodging), which causes yield loss. Another revolution was based on
hybridization between different inbred genotypes, which enhanced growth
and productivity, and also facilitated stacking disease resistance genes in
hybrid crops, such as maize, rice and tomato.

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Fig. 2. Antiflorigen mutations revolutionized multiple crops. (A) The tomato self pruning (sp) mutant (right) has
a compact ‘determinate’ growth habit with a burst of flowering and fruit production (inset) compared to the
continuous ‘indeterminate’ vine-like growth of classical cultivars (left) and their wild ancestors, (B) Similar benefits
for soybean came from mutations in the orthologous gene (determinate stem, dt1), (C) The cotton sp mutant
(Gbsp) has determinate shoots that result in the ‘clustered boll’ trait. All three mutants provide shorter stature with
multiple agronomic adaptations. Soybean images courtesy of J. Ma. Cotton images courtesy of T. Zhang.

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Fig. 3. Dwarfing mutations of the Green Revolution. (A) Wheat is a
hexaploid plant, and homeologues of the Reduced height-1 (Rht-1) genes
encode DELLA proteins that repress GA hormone signaling. Different
dominant alleles of the Rht-B1 and Rht-D1 homeologues that disrupt
DELLA protein degradation provide a range of reduced stem lengths and
plant height, which can further vary with genetic background. The semi-
dwarf Rht-B1b and Rht-D1b alleles (yellow, bold) are now found in the
majority of wheat varieties. Image courtesy of S. Thomas, (B) Step-
changes in plant stature (white arrows), which are further tuned by genetic
modifiers (black arrows), were the basis for the Green Revolution. Shown
is a model of yield that can be harvested under high nutrient field
conditions (harvestable yield) in relation to plant height. Tall plants that
were typical prior to the Green Revolution suffered from lodging when
fertilized, causing a loss of harvestable yield (blue area). Introducing and
breeding around (black arrows) the semidwarf Rht-B1b and Rht-D1b
mutant alleles resulted in optimal varieties with reduced lodging and a
doubling of harvestable yield.

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Fig. 4. Generalized scheme for generating targeted variation. Mutations in protein-coding
sequences provide mostly loss-of-function alleles that are likely to have qualitative phenotypic
consequences (notwithstanding genetic redundancy). Mutating introns or cis-regulatory regions
can alter expression, resulting in weaker alleles with a range of quantitative effects. When
combined with phenotypic screens, desirable alleles can be selected.

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 Fig. 5. Model of crop adaption for specific needs. Some crops make use
of vegetative parts of the plant, which could be optimized by delaying

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flowering. In contrast, adapting crops for very short seasons or
restricted growth space requires rapid flowering and the associated
growth arrest that limits plant size. Curves reflect the phenotypic space
that must be explored to select the optimum for specific needs. The
shape of the curve and its optimal points will shift depending on the
crop and growth conditions.

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Revolutions in agriculture chart a course for targeted breeding of old and new crops
Yuval Eshed and Zachary B. Lippman

published online September 5, 2019originally published online September 5, 2019

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