Root systems develop different root types that individually sense cues from their local environment and integrate this information with systemic signals. This complex multi-dimensional amalgam of inputs enables continuous adjustment of root growth rates, direction, and metabolic activity that define a dynamic physical network. Current methods for analyzing root biology balance physiological relevance with imaging capability. To bridge this divide, we developed an integrated-imaging system called Growth and Luminescence Observatory for Roots (GLO-Roots) that uses luminescence-based reporters to enable studies of root architecture and gene expression patterns in soil-grown, light-shielded roots. We have developed image analysis algorithms that allow the spatial integration of soil properties, gene expression, and root system architecture traits. We propose GLO-Roots as a system that has great utility in presenting environmental stimuli to roots in ways that evoke natural adaptive responses and in providing tools for studying the multi-dimensional nature of such processes.DOI: http://dx.doi.org/10.7554/eLife.07597.001
The phytochrome (phy) family of red and far-red photoreceptors provides plants with critical information about their surrounding environment and can signal downstream developmental and physiological changes. Neighboring plants compete for limited light resources, and their presence is detected by the phytochrome photoreceptors as a reduced ratio of red: far-red light. One common response to shade is increased elongation of petioles and internodes to compete with their neighbors. While the phytochrome family, phyB in particular, has been well studied in Arabidopsis, information about the other phytochrome family members is limited, especially in sympodial crop plants such as tomato, that have a very different architecture from that of the model plant. To study the tomato phytochrome family we took advantage of several existing mutants and generated an artificial miRNA (amiRNA) line to target SlPHYE, the remaining phytochrome B subfamily member with no currently available mutant line. Here, we characterize internode elongation and shade avoidance phenotypes of the SlPHYE amiRNA line (PHYE amiRNA). In addition, higher order phytochrome subfamily B mutants were generated with the PHYE amiRNA line to investigate the role of SlphyE within the phyB subfamily. We find that the PHYE amiRNA line has no detectable phenotype on its own, however in higher order combinations with SlphyB1 and/or SlphyB2 there are notable defects in shade avoidance. Most notably, we find that the triple mutant combination of SlPHYE amiRNA, SlphyB1, and SlphyB2 has a phenotype that is much stronger than the SlphyB1 SlphyB2 double, showing constitutive shade avoidance and little to no response to shade. This indicates that SlphyE is required for the shade avoidance response in the absence of SlphyB1 and SlphyB2.
Summary A network of environmental inputs and internal signaling controls plant growth, development and organ elongation. In particular, the growth‐promoting hormone gibberellin (GA) has been shown to play a significant role in organ elongation. The use of tomato as a model organism to study elongation presents an opportunity to study the genetic control of internode‐specific elongation in a eudicot species with a sympodial growth habit and substantial internodes that can and do respond to external stimuli. To investigate internode elongation, a mutant with an elongated hypocotyl and internodes but wild‐type petioles was identified through a forward genetic screen. In addition to stem‐specific elongation, this mutant, named tomato internode elongated ‐1 (tie‐1) is more sensitive to the GA biosynthetic inhibitor paclobutrazol and has altered levels of intermediate and bioactive GAs compared with wild‐type plants. The mutation responsible for the internode elongation phenotype was mapped to GA2oxidase 7, a class III GA 2‐oxidase in the GA biosynthetic pathway, through a bulked segregant analysis and bioinformatic pipeline, and confirmed by transgenic complementation. Furthermore, bacterially expressed recombinant TIE protein was shown to have bona fide GA 2‐oxidase activity. These results define a critical role for this gene in internode elongation and are significant because they further the understanding of the role of GA biosynthetic genes in organ‐specific elongation.
Interactions between MADS box transcription factors are critical in the regulation of floral development, and shifting MADS box protein-protein interactions are predicted to have influenced floral evolution. However, precisely how evolutionary variation in protein-protein interactions affects MADS box protein function remains unknown. To assess the impact of changing MADS box protein-protein interactions on transcription factor function, we turned to the grasses, where interactions between B-class MADS box proteins vary. We tested the functional consequences of this evolutionary variability using maize (Zea mays) as an experimental system. We found that differential B-class dimerization was associated with subtle, quantitative differences in stamen shape. In contrast, differential dimerization resulted in large-scale changes to downstream gene expression. Differential dimerization also affected B-class complex composition and abundance, independent of transcript levels. This indicates that differential B-class dimerization affects protein degradation, revealing an important consequence for evolutionary variability in MADS box interactions. Our results highlight complexity in the evolution of developmental gene networks: changing protein-protein interactions could affect not only the composition of transcription factor complexes but also their degradation and persistence in developing flowers. Our results also show how coding change in a pleiotropic master regulator could have small, quantitative effects on development.
The abrupt origin and rapid diversification of the flowering plants presents what Darwin called "an abominable mystery". Floral diversification was a key factor in the rise of the flowering plants, but the molecular underpinnings of floral diversity remain mysterious. To understand the molecular biology underlying floral morphological evolution, genetic model systems are essential for rigorously testing gene function and gene interactions. Most model plants are eudicots, while in the monocots genetic models are almost entirely restricted to the grass family. Likely because grass flowers are diminutive and specialized for wind pollination, grasses have not been a major focus in floral evo-devo research. However, while grass flowers do not exhibit any of the raucous morphological diversification characteristic of the orchids, there is abundant floral variation in the family. Here, we discuss grass flower diversity, and review what is known about the developmental genetics of this diversity. In particular, we focus on three aspects of grass flower evolution: (1) the evolution of a novel organ identity-the lodicule; (2) lemma awns and their diversity; and (3) the convergent evolution of sexual differentiation. The combination of morphological diversity in the grass family at large and genetic models spread across the family provides a powerful framework for attaining deep understanding of the molecular genetics of floral evolution.
Root systems develop different root types that individually sense eues from their local environment and integrate them with systemic signais. This complex multi-dimensional amalgam of inputs leads to continuous adjustment of root growth rates, direction and metabolic activity to define a dynamic physical network. Current methods for analyzing root biology balance physiological relevance with imaging capability. To bridge this divide, we developed an integrated imaging system called Growth and Luminescence Observatory for Roots (GLO-Roots) that uses luminescence-based reporters to enable studies of root architecture and gene expression patterns in soil-grown, light-shielded roots. We have developed image analysis algorithms that allow the spatial intgration of soil properties such as soil moisture with root traits. We propose GLO-Roots as a system that has great utility in both presenting environmental stimuli to roots in ways that evoke natural adaptive responses, and in providing tools for developing a multi-dimensional understanding of such processes.
The B-class MADS-box transcription factors STERILE TASSEL SILKY EAR1 (STS1) and SILKY1 (SI1) specify floral organ identity in the grass Zea mays (maize). STS1 and SI1 bind DNA as obligate heterodimers. Obligate heterodimerization between STS1 and SI1 homologs, although common in flowering plants, arose very recently in the grass family. This recent emergence of obligate heterodimerization from STS1 homodimerization provided an opportunity to test the consequences of evolutionary shifts in MADS-box protein-protein interactions. We tested the ability of evolutionary variation in STS1 dimerization to impact floral development, downstream gene regulation, and protein complex formation in maize. We found that STS1 hetero-vs. homodimerization had subtle effects on protein localization and stamen development. In contrast, differential STS1 dimerization resulted in largescale changes to gene expression and protein complex composition. We identified kinases and proteins involved in ubiquitylation as candidate interactors with MADS-box proteins, and found that STS1 was phosphorylated, and in a complex with ubiquitylated proteins. In addition, we found that STS1 homodimers were more abundant than STS1-SI1 heterodimers, independent of RNA levels. Thus, differential dimerization can affect both protein degradation dynamics and combinatorial assembly of MADS-box protein complexes. Our results highlight the robustness of floral development to some molecular change, which may contribute to the evolvability of floral form. Significance StatementInteractions between transcription factors can alter downstream gene expression patterns and, in turn, organismal development. In plants, MADS-box transcription factors specify floral organ identity as part of large complexes. Shifting interactions between MADS-box proteins have been proposed as drivers in the evolution of the flower, and in the diversification of floral form. However, the functional consequences of changes to individual MADS-box protein-protein interactions are unknown. Here, we show that floral development is subtly affected by altered transcription factor protein-protein interactions. We also show that shifting transcription factor interactions can contribute to differential protein degradation. This reveals an important consequence for evolutionary variation in transcription factor interactions, and adds a new layer of complexity to the evolution of developmental gene networks.
Crop engineering and de novo domestication using genome editing are new frontiers in agriculture. However, outside of well-studied crops and model systems, prioritizing engineering targets remains challenging. Evolution can serve as our guide, revealing high-priority genes with deeply conserved roles. Indeed,GRASSY TILLERS1(GT1),SIX-ROWED SPIKE1(VRS1), and their homologs have repeatedly been targets of selection in domestication and evolution. This repeated selection may be because these genes have an ancient, conserved role 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 CRISPR-Cas9 gene editing and mutant analysis.GT1andVRS1have roles in floral development in maize and barley, respectively. Grass flowers are borne in branching structures called spikelets. In maize spikelets, carpels are suppressed in half of all initiated ear flowers. These spikelets can only produce single grains. We show thatgt1; vrs1-like1(vrl1) mutants have derepressed carpels in ear flowers. Importantly, these plants can produce two grains per spikelet. In brachypodium,bdgt1; bdvrl1mutants have more branches, spikelets, and flowers than wildtype plants, indicating conserved roles forGT1andVRS1homologs in growth suppression. Indeed, maizeGT1can suppress growth inArabidopsis thaliana, separated from the grasses by ca. 160 million years of evolution. Thus,GT1andVRS1maintain their potency as growth regulators across vast timescales and in distinct developmental contexts. Modulating the activity of these and other conserved genes may be critical in crop engineering.
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