Phenylpropanoid metabolism is one of the most important metabolisms in plants, yielding more than 8,000 metabolites contributing to plant development and plant-environment interplay. Phenylpropanoid metabolism materialized during the evolution of early freshwater algae that were initiating terrestrialization and land plants have evolved multiple branches of this pathway, which give rise to metabolites including lignin, flavonoids, lignans, phenylpropanoid esters, hydroxycinnamic acid amides, and sporopollenin. Recent studies have revealed that many factors participate in the regulation of phenylpropanoid metabolism, and modulate phenylpropanoid homeostasis when plants undergo successive developmental processes and are subjected to stressful environments. In this review, we summarize recent progress on elucidating the contribution of phenylpropanoid metabolism to the coordination of plant development and plant-environment interaction, and metabolic flux redirection among diverse metabolic routes. In addition, our review focuses on the regulation of phenylpropanoid metabolism at the transcriptional, post-transcriptional, post-translational, and epigenetic levels, and in response to phytohormones and biotic and abiotic stresses.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/jipb.13054

Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions.

Anthocyanins play a variety of adaptive roles in both vegetative tissues and reproductive organs of plants. The broad functionality of these compounds requires sophisticated regulation of the anthocyanin biosynthesis pathway to allow proper localization, timing, and optimal intensity of pigment deposition. While it is well-established that the committed steps of anthocyanin biosynthesis are activated by a highly conserved MYB-bHLH-WDR (MBW) protein complex in virtually all flowering plants, anthocyanin repression seems to be achieved by a wide variety of protein and small RNA families that function in different tissue types and in response to different developmental, environmental, and hormonal cues. In this review, we survey recent progress in the identification of anthocyanin repressors and the characterization of their molecular mechanisms. We find that these seemingly very different repression modules act through a remarkably similar logic, the so-called 'double-negative logic'. Much of the double-negative regulation of anthocyanin production involves signal-induced degradation or sequestration of the repressors from the MBW protein complex. We discuss the functional and evolutionary advantages of this logic design compared with simple or sequential positive regulation. These advantages provide a plausible explanation as to why plants have evolved so many anthocyanin repressors.

Repressors of anthocyanin biosynthesis.

Contents Summary 694 I. Introduction 694 II. The system 695 III. Regulation of carotenoid pigmentation 695 IV. Formation of periodic pigmentation patterns 696 V. Developmental genetics of corolla tube formation and elaboration 697 VI. Molecular basis of floral trait variation underlying pollinator shift 698 VII. Outlook 699 Acknowledgements 699 References 699 SUMMARY: Monkeyflowers (Mimulus) have long been recognized as a classic ecological and evolutionary model system. However, only recently has it been realized that this system also holds great promise for studying the developmental genetics and evo-devo of important plant traits that are not found in well-established model systems such as Arabidopsis. Here, I review recent progress in four different areas of plant research enabled by this new model, including transcriptional regulation of carotenoid biosynthesis, formation of periodic pigmentation patterns, developmental genetics of corolla tube formation and elaboration, and the molecular basis of floral trait divergence underlying pollinator shift. These examples suggest that Mimulus offers ample opportunities to make exciting discoveries in plant development and evolution.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.15560

Monkeyflowers (Mimulus): new model for plant developmental genetics and evo‐devo

Anthocyanin biosynthesis is mainly controlled by MYB-bHLH-WD40 (MBW) complexes that modulate the expression of anthocyanin biosynthetic genes (ABGs). The MYB regulators involved in anthocyanin biosynthesis arose early during plant evolution and thus might function divergently in different evolutionary lineages. Although the anthocyanin-promoting R2R3-MYB regulators in eudicots have been comprehensively explored, little consensus has been reached about functional discrepancies versus conservation among MYB regulators from different plant lineages. Here, we integrated transcriptome analysis, gene expression profiles, gain-of-function experiments and transient protoplast transfection assays to functionally characterize the monocot Freesia hybrida anthocyanin MYB regulator gene FhPAP1, which showed correlations with late ABGs. FhPAP1 could activate ABGs as well as TT8-clade genes FhTT8L, AtTT8 and NtAN1 when overexpressed in Freesia, Arabidopsis and tobacco, respectively. Consistently, FhPAP1 could interact with FhTT8L and FhTTG1 to form the conserved MBW complex and shared similar target genes with its orthologs from Arabidopsis. Most prominently, FhPAP1 displayed higher transactivation capacity than its homologs in Arabidopsis and tobacco, which was instantiated in its powerful regulation on ABGs. Moreover, we found that FhPAP1 might be the selected gene during the domestication and rapid evolution of the wild Freesia species to generate intensive flower pigmentation. These results showed that while the MBW complex was highly evolutionarily conserved between tested monocot and core eudicot plants, participating MYB regulators showed functional differences in transactivation capacity according to their activation domain and played important roles in the flower coloration domestication and evolution of angiosperms.

The Conserved and Particular Roles of the R2R3-MYB Regulator FhPAP1 from Freesia hybrida in Flower Anthocyanin Biosynthesis

Floral anthocyanin has multiple ecological and economic values, its biosynthesis largely depends on the conserved MYB-bHLH-WD40 (MBW) activation complex and MYB repressors hierarchically with the MBW complex. In contrast to eudicots, the MBW regulatory network model has not been addressed in monocots because of the lack of a suitable system, as grass plants exhibit monotonous floral pigmentation patterns. Presently, the MBW regulatory network was investigated in a non-grass monocot plant, Freesia hybrida. FhMYB27 and FhMYBx with different functional manners were confirmed to be anthocyanin related R2R3 and R3 MYB repressors, respectively. Particularly, FhMYBx could obstruct the formation of positive MBW complex by titrating bHLH proteins, whereas FhMYB27 mainly defected the activator complex into suppressor via its repression domains in C-terminus. Furthermore, the hierarchical and feedback regulatory loop was verified, indicating the synergistic and sophisticated regulatory network underlying Freesia anthocyanin biosynthesis was quite similar to that reported in eudicot plants.

/pdf/myb-repressors-and-mbw-activation-complex-collaborate-to-4oonr7p1rm.pdf

MYB repressors and MBW activation complex collaborate to fine-tune flower coloration in Freesia hybrida.

Two MYB Proteins in a Self-Organizing Activator-Inhibitor System Produce Spotted Pigmentation Patterns.

Style length is a major determinant of breeding strategies in flowering plants and can vary dramatically between and within species. However, little is known about the genetic and developmental control of style elongation. We characterized the role of two classes of leaf adaxial-abaxial polarity factors, SUPPRESSOR OF GENE SILENCING3 (SGS3) and the YABBY family transcription factors, in the regulation of style elongation in Mimulus lewisii. We also examined the spatiotemporal patterns of auxin response during style development. Loss of SGS3 function led to reduced style length via limiting cell division, and downregulation of YABBY genes by RNA interference resulted in shorter styles by decreasing both cell division and cell elongation. We discovered an auxin response minimum between the stigma and ovary during the early stages of pistil development that marks style differentiation. Subsequent redistribution of auxin response to this region was correlated with style elongation. Auxin response was substantially altered when both SGS3 and YABBY functions were disrupted. We suggest that auxin signaling plays a central role in style elongation and that the way in which auxin signaling controls the different cell division and elongation patterns underpinning natural style length variation is a major question for future research.

The leaf polarity factors SGS3 and YABBYs regulate style elongation through auxin signaling in Mimulus lewisii

Many organisms exhibit visually striking spotted or striped pigmentation patterns. Turing9s reaction-diffusion model postulates that such periodic pigmentation patterns form when a local autocatalytic feedback loop and a long-range inhibitory feedback loop interact. At its simplest, this network only requires one self-activating activator that also activates a repressor, which inhibits the activator and diffuses to neighboring cells. However, the molecular activators and repressors fully fitting this versatile model remain elusive. Here, we characterize an R2R3-MYB activator and an R3-MYB repressor in monkeyflowers that correspond to Turing9s model and explain how periodic anthocyanin spots form. Notably, disrupting this pattern impacts pollinator visitation. Thus, subtle changes in simple reaction-diffusion networks are likely essential contributors to the evolution of the remarkable diversity of periodic pigmentation patterns in flowers.

https://www.biorxiv.org/content/biorxiv/early/2018/08/30/403600.full.pdf

Jingjian Li

Papers

Two MYB Proteins in a Self-Organizing Activator-Inhibitor System Produce Spotted Pigmentation Patterns.

The leaf polarity factors SGS3 and YABBYs regulate style elongation through auxin signaling in Mimulus lewisii

Formation of periodic pigment spots by the reaction-diffusion mechanism