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. Although step changes based on serendipitous mutations in these hormone systems laid the foundation, genetic and agronomic tuning were 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 could help to meet the future needs of the human diet and promote sustainable agriculture.
Leaves are flat determinate organs derived from indeterminate shoot apical meristems. The presence of a specific leaf meristem is debated, as anatomical features typical of meristems are not present ...in leaves. Here we demonstrate that multiple NGATHA (NGA) and CINCINNATA-class-TCP (CIN-TCP) transcription factors act redundantly, shortly after leaf initiation, to gradually restrict the activity of a leaf meristem in
to marginal and basal domains, and that their absence confers persistent marginal growth to leaves, cotyledons and floral organs. Following primordia initiation, the restriction of the broadly acting leaf meristem to the margins is mediated by the juxtaposition of adaxial and abaxial domains and maintained by WOX homeobox transcription factors, whereas other marginal elaboration genes are dispensable for its maintenance. This genetic framework parallels the morphogenetic program of shoot apical meristems and may represent a relic of an ancestral shoot system from which seed plant leaves evolved.
The leaves of seed plants evolved from a primitive shoot system and are generated as determinate dorsiventral appendages at the flanks of radial indeterminate shoots. The remarkable variation of ...leaves has remained a constant source of fascination, and their developmental versatility has provided an advantageous platform to study genetic regulation of subtle, and sometimes transient, morphological changes. Here, we describe how eudicot plants recruited conserved shoot meristematic factors to regulate growth of the basic simple leaf blade and how subsets of these factors are subsequently re-employed to promote and maintain further organogenic potential. By comparing tractable genetic programs of species with different leaf types and evaluating the pros and cons of phylogenetic experimental procedures, we suggest that simple and compound leaves, and, by the same token, leaflets and serrations, are regulated by distinct ontogenetic programs. Finally, florigen, in its capacity as a general growth regulator, is presented as a new upper-tier systemic modulator in the patterning of compound leaves.
Divergence of gene function is a hallmark of evolution, but assessing functional divergence over deep time is not trivial. The few alleles available for cross-species studies often fail to expose the ...entire functional spectrum of genes, potentially obscuring deeply conserved pleiotropic roles. Here, we explore the functional divergence of WUSCHEL HOMEOBOX9 (WOX9), suggested to have species-specific roles in embryo and inflorescence development. Using a cis-regulatory editing drive system, we generate a comprehensive allelic series in tomato, which revealed hidden pleiotropic roles for WOX9. Analysis of accessible chromatin and conserved cis-regulatory sequences identifies the regions responsible for this pleiotropic activity, the functions of which are conserved in groundcherry, a tomato relative. Mimicking these alleles in Arabidopsis, distantly related to tomato and groundcherry, reveals new inflorescence phenotypes, exposing a deeply conserved pleiotropy. We suggest that targeted cis-regulatory mutations can uncover conserved gene functions and reduce undesirable effects in crop improvement.
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•Targeted cis-regulatory mutagenesis uncovered hidden pleiotropy in a plant homeobox gene•Different pleiotropic functions can be mapped to specific cis-regulatory regions•Pleiotropy and cis-regulatory control sequences are conserved in related species•Pleiotropy, but not cis-regulatory structure, is conserved in distantly related plants
Functional dissections of cis-regulatory DNA suggest a conserved hidden pleiotropy widespread in plant evolution that has implications for the utilization of genome editing in agriculture
Structural variants (SVs) underlie important crop improvement and domestication traits. However, resolving the extent, diversity, and quantitative impact of SVs has been challenging. We used ...long-read nanopore sequencing to capture 238,490 SVs in 100 diverse tomato lines. This panSV genome, along with 14 new reference assemblies, revealed large-scale intermixing of diverse genotypes, as well as thousands of SVs intersecting genes and cis-regulatory regions. Hundreds of SV-gene pairs exhibit subtle and significant expression changes, which could broadly influence quantitative trait variation. By combining quantitative genetics with genome editing, we show how multiple SVs that changed gene dosage and expression levels modified fruit flavor, size, and production. In the last example, higher order epistasis among four SVs affecting three related transcription factors allowed introduction of an important harvesting trait in modern tomato. Our findings highlight the underexplored role of SVs in genotype-to-phenotype relationships and their widespread importance and utility in crop improvement.
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•Long-read sequencing of 100 tomato genomes uncovered 238,490 structural variants•Transposons underlie many SVs, and SV hotspots revealed large introgressions•SVs associated with genes are predictive of population-scale changes in expression•New genome assemblies resolved complex breeding QTLs caused by SVs
Comprehensive structural variant identification in tomato genomes allows insight into the evolution and domestication of tomato and serves as a resource for phenotype-directed breeding.
Naturally occurring genetic variation in the universal florigen flowering pathway has produced major advancements in crop domestication. However, variants that can maximize crop yields may not exist ...in natural populations. Here we show that tomato productivity can be fine-tuned and optimized by exploiting combinations of selected mutations in multiple florigen pathway components. By screening for chemically induced mutations that suppress the bushy, determinate growth habit of field tomatoes, we isolated a new weak allele of the florigen gene SINGLE FLOWER TRUSS (SFT) and two mutations affecting a bZIP transcription factor component of the 'florigen activation complex' (ref. 11). By combining heterozygous mutations, we pinpointed an optimal balance of flowering signals, resulting in a new partially determinate architecture that translated to maximum yields. We propose that harnessing mutations in the florigen pathway to customize plant architecture and flower production offers a broad toolkit to boost crop productivity.
•A gradual process of meristem maturation precedes the floral transition.•Reproductive shoot systems—inflorescences—come in continuous forms.•Tomato and related species vary in inflorescences and ...meristem maturation processes.•Disrupting maturation regulators has species-specific impacts on inflorescences.•Molecular dissection of maturation may reveal commonalities among diverse shoot architectures.
Plant apical meristems (AMs) grow continuously by delicately balancing cells leaving at the periphery to form lateral organs with slowly dividing central domain cells that replenish reservoirs of pluripotent cells. This balance can be modified by signals originating from within and outside the meristem, and their integration results in a gradual maturation process that often culminates with the meristem differentiating into a flower. Accompanying this ‘meristem maturation’ are changes in spacing and size of lateral organs and in rates at which lateral meristems are released from apical dominance. Modulation of distinct meristem maturation parameters through environmental and genetic changes underlies the remarkable diversity of shoot architectures. Here, we discuss recent studies relating the dynamics of meristem maturation with organization of floral branching systems—inflorescences—in the nightshades. From this context, we suggest general principles on how factors coordinating meristem maturation impact shoot organization more broadly.
Domestication of upland cotton (Gossypium hirsutum) converted it from a lanky photoperiodic perennial to a day-neutral annual row-crop. Residual perennial traits, however, complicate irrigation and ...crop management, and more determinate architectures are desired. Cotton simultaneously maintains robust monopodial indeterminate shoots and sympodial determinate shoots. We questioned if and how the FLOWERING LOCUS T/SINGLE FLOWER TRUSS (SFT)-like and TERMINAL FLOWER1/SELF-PRUNING (SP)-like genes control the balance of monopodial and sympodial growth in a woody perennial with complex growth habit.
Virus-based manipulation of GhSP and GhSFT expression enabled unprecedented functional analysis of cotton development.
GhSP maintains growth in all apices; in its absence, both monopodial and sympodial branch systems terminate precociously. GhSFT encodes a florigenic signal stimulating rapid onset of sympodial branching and flowering in side shoots of wild photoperiodic and modern day-neutral accessions. High florigen concentrations did not alter monopodial apices, implying that once a cotton apex is SP-determined, it cannot be reset by florigen. GhSP is also essential to establish and maintain cambial activity.
Dynamic changes in GhSFT and GhSP levels navigate meristems between monopodial and sympodial programs in a single plant. SFT and SP influenced cotton domestication and are ideal targets for further agricultural optimization.
Plant shoots display indeterminate growth, while their evolutionary decedents, the leaves, are determinate. Determinate leaf growth is conditioned by the CIN-TCP transcription factors, which promote ...leaf maturation and are negatively regulated by miR319 in leaf primordia. Here we show that CIN-TCPs reduce leaf sensitivity to cytokinin (CK), a phytohormone implicated in inhibition of differentiation in the shoot. We identify the SWI/SNF chromatin remodeling ATPase BRAHMA (BRM) as a genetic mediator of CIN-TCP activities and CK responses. An interactome screen further revealed that SWI/SNF complex components including BRM preferentially interacted with basic-helix-loop-helix (bHLH) transcription factors and the bHLH-related CIN-TCPs. Indeed, TCP4 and BRM interacted in planta. Both TCP4 and BRM bound the promoter of an inhibitor of CK responses, ARR16, and induced its expression. Reconstituting ARR16 levels in leaves with reduced CIN-TCP activity restored normal growth. Thus, CIN-TCP and BRM together promote determinate leaf growth by stage-specific modification of CK responses.
► CIN-TCP transcription factors such as TCP4 modulate Arabidopsis leaf response to CK ► A genetic screen identifies the chromatin remodeler BRM as required for TCP4 action ► An interactome screen identifies TCPs as preferential BRM interactors ► TCP4 and BRM directly induce ARR16, a negative CK response regulator
CIN-TCP transcription factors and the hormone cytokinin (CK) play opposing roles in leaf maturation. Efroni et al. show that the CIN-TCP factor TCP4 interacts with SWI/SNF chromatin remodeler BRM to modulate sensitivity to CK. BRM and TCP4 induce the CK response inhibitor ARR16, determining leaf growth by stage-specific modification of CK responses.
The florigen paradigm implies a universal flowering-inducing hormone that is common to all flowering plants. Recent work identified FT orthologues as originators of florigen and their polypeptides as ...the likely systemic agent. However, the developmental processes targeted by florigen remained unknown. Here we identify local balances between SINGLE FLOWER TRUSS (SFT), the tomato precursor of florigen, and SELF-PRUNING (SP), a potent SFT-dependent SFT inhibitor as prime targets of mobile florigen. The graft-transmissible impacts of florigen on organ-specific traits in perennial tomato show that in addition to import by shoot apical meristems, florigen is imported by organs in which SFT is already expressed. By modulating local SFT/SP balances, florigen confers differential flowering responses of primary and secondary apical meristems, regulates the reiterative growth and termination cycles typical of perennial plants, accelerates leaf maturation, and influences the complexity of compound leaves, the growth of stems and the formation of abscission zones. Florigen is thus established as a plant protein functioning as a general growth hormone. Developmental interactions and a phylogenetic analysis suggest that the SFT/SP regulatory hierarchy is a recent evolutionary innovation unique to flowering plants.
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