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.

Flavonoids are major secondary metabolites derived from the plant phenylpropanoid pathway that play important roles in plant development and also have benefits for human health. So-called MBW ternary complexes involving R2R3-MYB and basic helix-loop-helix (bHLH) transcription factors along with WD-repeat proteins have been reported to regulate expression of the biosynthetic genes in the flavonoid pathway. MYB4 and its closest homolog MYB7 have been suggested to function as repressors of phenylpropanoid metabolism. However, the detailed mechanism by which they act has not been fully elucidated. Here, we show that Arabidopsis thaliana MYB4 and its homologs MYB7 and MYB32 interact with the bHLH transcription factors TT8, GL3 and EGL3 and thereby interfere with the transcriptional activity of the MBW complexes. In addition, MYB4 can also inhibit flavonoid accumulation by repressing expression of the gene encoding Arogenate Dehydratase 6 (ADT6), which catalyzes the final step in the biosynthesis of phenylalanine, the precursor for flavonoid biosynthesis. MYB4 potentially represses not only the conventional ADT6 encoding the plastidial enzyme but also the alternative isoform encoding the cytosolic enzyme. We suggest that MYB4 plays dual roles in modulating the flavonoid biosynthetic pathway in Arabidopsis.

https://onlinelibrary.wiley.com/doi/epdf/10.1111/tpj.14570

Arabidopsis MYB4 plays dual roles in flavonoid biosynthesis.

Drought stress induces anthocyanin biosynthesis in many plant species, but the underlying molecular mechanism remains unclear. Ethylene response factors (ERFs) play key roles in plant growth and various stress responses, including affecting anthocyanin biosynthesis. Here, we characterized an ERF protein, MdERF38, which is involved in drought stress-induced anthocyanin biosynthesis. Biochemical and molecular analyses showed that MdERF38 interacted with MdMYB1, a positive modulator of anthocyanin biosynthesis, and facilitated the binding of MdMYB1 to its target genes. Therefore, MdERF38 promoted anthocyanin biosynthesis in response to drought stress. Furthermore, we found that MdBT2, a negative modulator of anthocyanin biosynthesis, decreased MdERF38-promoted anthocyanin biosynthesis by accelerating the degradation of the MdERF38 protein. In summary, our data provide a mechanism for drought stress-induced anthocyanin biosynthesis that involves dynamic modulation of MdERF38 at both transcriptional and post-translational levels.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.14555

The ERF transcription factor MdERF38 promotes drought stress-induced anthocyanin biosynthesis in apple

Wounding stress leads to anthocyanin accumulation. However, the underlying molecular mechanism remains elusive. In this study, MdWRKY40 was found to promote wounding-induced anthocyanin biosynthesis in association with MdMYB1 and undergo MdBT2-mediated degradation in apple. We found that MdMYB1, a positive regulator of anthocyanin biosynthesis, was essential for the wounding-induced anthocyanin biosynthesis in apple. MdWRKY40 was identified as an MdMYB1-interacting protein, and enhanced the binding of MdMYB1 to its target genes in response to wounding. We found that MdBT2 interacted physically with MdWRKY40 and was involved in its degradation through the 26S proteasome pathway. Our results demonstrate that MdWRKY40 is a key modulator in the wounding-induced anthocyanin biosynthesis, which provides new insights into the regulation of wounding-induced anthocyanin biosynthesis at both the transcriptional and post-translational levels in apple.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.16008

MdWRKY40 promotes wounding‐induced anthocyanin biosynthesis in association with MdMYB1 and undergoes MdBT2‐mediated degradation

Salinity stress is one of the major threats to agricultural productivity across the globe Research in the past three decades, therefore, has focused on analyzing the effects of salinity stress on the plants Evidence gathered over the years supports the role of ethylene as a key regulator of salinity stress tolerance in plants This gaseous plant hormone regulates many vital cellular processes starting from seed germination to photosynthesis for maintaining the plants’ growth and yield under salinity stress Ethylene modulates salinity stress responses largely via maintaining the homeostasis of Na+/K+, nutrients, and reactive oxygen species (ROS) by inducing antioxidant defense in addition to elevating the assimilation of nitrates and sulfates Moreover, a cross-talk of ethylene signaling with other phytohormones has also been observed, which collectively regulate the salinity stress responses in plants The present review provides a comprehensive update on the prospects of ethylene signaling and its cross-talk with other phytohormones to regulate salinity stress tolerance in plants

https://www.mdpi.com/2218-273X/10/6/959/pdf

Ethylene: A Master Regulator of Salinity Stress Tolerance in Plants.

Phytohormone abscisic acid (ABA) induces anthocyanin biosynthesis; however, the underlying molecular mechanism is less known. In this study, we found that the apple MYB transcription factor MdMYB1 activated anthocyanin biosynthesis in response to ABA. Using a yeast screening technique, we isolated MdbZIP44, an ABA-induced bZIP transcription factor in apple, as a co-partner with MdMYB1. MdbZIP44 promoted anthocyanin accumulation in response to ABA by enhancing the binding of MdMYB1 to the promoters of downstream target genes. Furthermore, we identified MdBT2, a BTB protein, as an MdbZIP44-interacting protein. A series of molecular, biochemical, and genetic analysis suggested that MdBT2 degraded MdbZIP44 protein through the Ubiquitin-26S proteasome system, thus inhibiting MdbZIP44-modulated anthocyanin biosynthesis. Taken together, we reveal a novel working mechanism of MdbZIP44-mediated anthocyanin biosynthesis in response to ABA.

Apple bZIP transcription factor MdbZIP44 regulates abscisic acid-promoted anthocyanin accumulation.

It is known that ethylene signaling is involved in the regulation of the salt stress response. However, the molecular mechanism of ethylene-regulated salt stress tolerance remains largely unclear. In this study, an apple NAM ATAF CUC transcription factor, MdNAC047, was isolated and functionally characterized to be involved in ethylene-modulated salt tolerance. MdNAC047 gene was significantly induced by salt treatment and its overexpression conferred increased tolerance to salt stress and facilitated the release of ethylene. Quantitative real-time-PCR analysis demonstrated that overexpression of MdNAC047 increased the expression of ethylene-responsive genes. Electrophoretic mobility shift assay, yeast one-hybrid and dual-luciferase assays suggested that MdNAC047 directly binds to the MdERF3 (ETHYLENE RESPONSE FACTOR) promoter and activates its transcription. In addition, genetic analysis assays indicated that MdNAC047 regulates ethylene production at least partially in an MdERF3-dependent pathway. Overall, we found a novel 'MdNAC047-MdERF3-ethylene-salt tolerance' regulatory pathway, which provide new insight into the link between ethylene and salt stress.

An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response.

Jasmonate (JA) induces the biosynthesis of anthocyanin and proanthocyanidin. MdMYB9 is essential for modulating the accumulation of both anthocyanin and proanthocyanidin in apple, but the molecular mechanism for induction of anthocyanin and proanthocyanidin biosynthesis by JA is unclear. In this study, we discovered an apple telomere-binding protein (MdTRB1) to be the interacting protein of MdMYB9. A series of biological assays showed that MdTRB1 acted as a positive modulator of anthocyanin and proanthocyanidin accumulation, and is dependent on MdMYB9. MdTRB1 interacted with MdMYB9 and enhanced the activation activity of MdMYB9 to its downstream genes. In addition, we found that the JA signaling repressor MdJAZ1 interacted with MdTRB1 and interfered with the interaction between MdTRB1 and MdMYB9, therefore negatively modulating MdTRB1-promoted biosynthesis of anthocyanin and proanthocyanidin. These results show that the JAZ1-TRB1-MYB9 module dynamically modulates JA-mediated accumulation of anthocyanin and proanthocyanidin. Taken together, our data further expand the functional study of TRB1 and provide insights for further studies of the modulation of anthocyanin and proanthocyanidin biosynthesis by JA.

Jasmonate induces biosynthesis of anthocyanin and proanthocyanidin in apple by mediating the JAZ1-TRB1-MYB9 complex.

Apple MdERF4 negatively regulates salt tolerance by inhibiting MdERF3 transcription

Abscisic acid (ABA) is involved in the regulation of cold stress response, but its molecular mechanism remains to be elucidated. In this study, we demonstrated that the APETALA2/ethylene responsive factor (AP2/ERF) family protein MdABI4 positively regulates ABA-mediated cold tolerance in apple. We found that MdABI4 interacts with MdICE1, a key regulatory protein involved in the cold stress response, and enhances the transcriptional function of MdICE1 on its downstream target gene MdCBF1, thus improving ABA-mediated cold tolerance. Apple jasmonate-ZIM domain (JAZ) proteins MdJAZ1 and MdJAZ2 negatively modulate MdABI4-improved cold tolerance by interacting with the MdABI4 protein. Further research showed that MdJAZ1 and MdJAZ2 interfere with the interaction between the MdABI4 and MdICE1 proteins. Together, our data revealed that MdABI4 integrates jasmonic acid (JA) and ABA signals to delicately modulate cold tolerance through the JAZ-ABI4-ICE1-CBF regulatory cascade in apple. These findings will provide insights into the crosstalk between JA and ABA signals in the cold stress response.

Rui-Rui Xu

Papers

Apple bZIP transcription factor MdbZIP44 regulates abscisic acid-promoted anthocyanin accumulation.

An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response.

Jasmonate induces biosynthesis of anthocyanin and proanthocyanidin in apple by mediating the JAZ1-TRB1-MYB9 complex.

Apple MdERF4 negatively regulates salt tolerance by inhibiting MdERF3 transcription

ABI4 interacts with ICE1 and JAZ proteins to regulate abscisic acid signaling-mediated cold tolerance in apple.