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Abstract Cryptic genetic variants exert minimal phenotypic effects alone but are hypothesized to form a vast reservoir of genetic diversity driving trait evolvability through epistatic interactions^1–3. This classical theory has been reinvigorated by pan-genomics, which is revealing pervasive variation within gene families,cis-regulatory regions and regulatory networks^4–6. Testing the ability of cryptic variation to fuel phenotypic diversification has been hindered by intractable genetics, limited allelic diversity and inadequate phenotypic resolution. Here, guided by natural and engineeredcis-regulatory cryptic variants in a paralogous gene pair, we identified additional redundanttransregulators, establishing a regulatory network controlling tomato inflorescence architecture. By combining coding mutations withcis-regulatory alleles in populations segregating for all four network genes, we generated 216 genotypes spanning a wide spectrum of inflorescence complexity and quantified branching in over 35,000 inflorescences. Analysis of this high-resolution genotype–phenotype map using a hierarchical model of epistasis revealed a layer of dose-dependent interactions within paralogue pairs enhancing branching, culminating in strong, synergistic effects. However, we also identified a layer of antagonism between paralogue pairs, whereby accumulating mutations in one pair progressively diminished the effects of mutations in the other. Our results demonstrate how gene regulatory network architecture and complex dosage effects from paralogue diversification converge to shape phenotypic space, producing the potential for both strongly buffered phenotypes and sudden bursts of phenotypic change. 

Summary Replicated trait evolution can provide insights into the mechanisms underlying the evolution of biodiversity. One example of replicated evolution is the awn, an organ elaboration in grass inflorescences.Awns are likely homologous to leaf blades. We hypothesized that awns have evolved repeatedly because a conserved leaf blade developmental program is continuously activated and suppressed over the course of evolution, leading to the repeated emergence and loss of awns. To evaluate predictions arising from our hypothesis, we used ancestral state estimations, comparative genetics, anatomy, and morphology to trace awn evolution.We discovered that awned lemmas that evolved independently share similarities in developmental trajectory. In addition, in two species with independently derived awns and differing awn morphologies (Brachypodium distachyonandAlopecurus myosuroides), we found that orthologs of theYABBYtranscription factor geneDROOPING LEAFare required for awn initiation. Our analyses of awn development inBrachypodium distachyon,Alopecurus myosuroides, andHolcus lanatusalso revealed that differences in the relative expansion of awned lemma compartments can explain diversity in awn morphology at maturity.Our results show that developmental conservation can underlie replicated evolution and can potentiate the evolution of morphological diversity. 

ABSTRACT Cryptic genetic variants exert minimal or no phenotypic effects alone but have long been hypothesized to form a vast, hidden reservoir of genetic diversity that drives trait evolvability through epistatic interactions. This classical theory has been reinvigorated by pan-genome sequencing, which has revealed pervasive variation within gene families and regulatory networks, including extensive cis-regulatory changes, gene duplication, and divergence between paralogs. Nevertheless, empirical testing of cryptic variation’s capacity to fuel phenotypic diversification has been hindered by intractable genetics, limited allelic diversity, and inadequate phenotypic resolution. Here, guided by natural and engineered cis-regulatory cryptic variants in a recently evolved paralogous gene pair, we identified an additional pair of redundant trans regulators, establishing a regulatory network that controls tomato inflorescence architecture. By combining coding mutations with a cis-regulatory allelic series in populations segregating for all four network genes, we systematically constructed a collection of 216 genotypes spanning the full spectrum of inflorescence complexity and quantified branching in over 27,000 inflorescences. Analysis of the resulting high-resolution genotype-phenotype map revealed a layer of dose-dependent interactions within paralog pairs that enhances branching, culminating in strong, synergistic effects. However, we also uncovered an unexpected layer of antagonism between paralog pairs, where accumulating mutations in one pair progressively diminished the effects of mutations in the other. Our results demonstrate how gene regulatory network architecture and complex dosage effects from paralog diversification converge to shape phenotypic space under a hierarchical model of epistatic interactions. Given the prevalence of paralog evolution in genomes, we propose that paralogous cryptic variation within regulatory networks elicits hierarchies of epistatic interactions, catalyzing bursts of phenotypic change. Keyword:cryptic mutations, paralogs, redundancy, cis-regulatory, tomato, inflorescence, gene regulatory network, modeling, epistasis 

Synopsis How did plant sexuality come to so hauntingly resemble human sexual formations? How did plant biology come to theorize plant sexuality with binary formulations of male/female, sex/gender, sperm/egg, active males and passive females—all of which resemble western categories of sex, gender, and sexuality? Tracing the extant language of sex and sexuality in plant reproductive biology, we examine the histories of science to explore how plant reproductive biology emerged historically from formations of colonial racial and sexual politics and how evolutionary biology was premised on the imaginations of racialized heterosexual romance. Drawing on key examples, the paper aims to (un)read plant sexuality and sexual anatomy and bodies to imagine new possibilities for plant sex, sexualities, and their relationalities. In short, plant sex and sexuality are not two different objects of inquiry but are intimately related—it is their inter-relation that is the focus of this essay. One of the key impulses from the humanities that we bring to this essay is a careful consideration of how terms and terminologies are related to each other historically and culturally. In anthropomorphizing plants, if plant sexuality were modeled on human sexual formations, might a re-imagination of plant sexuality open new vistas for the biological sciences? While our definitions of plant sexuality will always be informed by contemporary society and culture, interrogating the histories of our theories and terminologies can help us reimagine a biology that allows for new and more accurate understandings of plants, plant biology, and the evolution of reproduction. 

Every spring, something seemingly miraculous happens in the woods in certain parts of the world—thousands of leaves burst from buds on bare tree branches, transforming the landscape from the browns and grays of winter to the bright greens of spring and summer. Although this process is most obvious in regions with drastic seasonal changes, seed plants all over the world regularly produce and lose leaves as they grow. How does this happen? Where do these leaves come from? The cells that make up these leaves are produced by a tiny cluster of cells called the shoot apical meristem. The cells in the shoot apical meristem have the potential to develop into various kinds of cells. Through cell division, meristem cells eventually produce all the above-ground parts of a plant, including leaves. In this article, we explain how meristems function and highlight how these tiny clusters of cells impact our day-to-day lives. We will also provide suggestions for observing meristems at work. 

Crop engineering and de novo domestication using gene editing are new frontiers in agriculture. However, outside of well-studied crops and model systems, prioritizing engineering targets remains challenging. Evolution can guide us, revealing genes with deeply conserved roles that have repeatedly been selected in the evolution of plant form. Homologs of the transcription factor genesGRASSY TILLERS1(GT1) andSIX-ROWED SPIKE1(VRS1) have repeatedly been targets of selection in domestication and evolution, where they repress growth in many developmental contexts. This suggests a conserved role for these genes in regulating growth repression. To test this, we determined the roles ofGT1andVRS1homologs in maize (Zea mays) and the distantly related grass brachypodium (Brachypodium distachyon) using gene editing and mutant analysis. In maize,gt1; vrs1-like1(vrl1) mutants have derepressed growth of floral organs. In addition,gt1; vrl1mutants bore more ears and more branches, indicating broad roles in growth repression. In brachypodium,Bdgt1;Bdvrl1mutants have more branches, spikelets, and flowers than wild-type plants, indicating conserved roles forGT1andVRS1homologs in growth suppression overca.59 My of grass evolution. Importantly, many of these traits influence crop productivity. Notably, maizeGT1can suppress growth in arabidopsis (Arabidopsis thaliana) floral organs, despiteca. 160 My of evolution separating the grasses and arabidopsis. Thus,GT1andVRS1maintain their potency as growth regulators across vast timescales and in distinct developmental contexts. This work highlights the power of evolution to inform gene editing in crop improvement. 

Grass inflorescence branching involves the integration of competing signals that regulate leaf and meristem growth.