Beronda L. Montgomery

Growth-defense tradeoffs in plants: A balancing act to optimize fitness

Growth-defense tradeoffs are thought to occur in plants due to resource restrictions, which demand prioritization towards either growth or defense, depending on external and internal factors. These tradeoffs have profound implications in agriculture and natural ecosystems, as both processes are vital for plant survival, reproduction, and, ultimately, plant fitness. While many of the molecular mechanisms underlying growth and defense tradeoffs remain to be elucidated, hormone crosstalk has emerged as a major player in regulating tradeoffs needed to achieve a balance. In this review, we cover recent advances in understanding growth-defense tradeoffs in plants as well as what is known regarding the underlying molecular mechanisms. Specifically, we address evidence supporting the growth-defense tradeoff concept, as well as known interactions between defense signaling and growth signaling. Understanding the molecular basis of these tradeoffs in plants should provide a foundation for the development of breeding strategies that optimize the growth-defense balance to maximize crop yield to meet rising global food and biofuel demands.

Sensing the light: photoreceptive systems and signal transduction in cyanobacteria

Photosynthetic prokaryotes have highly developed abilities to detect and react to environmental signals. Light sensing is one of the most important capabilities of organisms that use light for photosynthesis and photomorphogenesis. This review addresses photoreception in cyanobacteria from the perception of light through the physiological responses observed in response to light‐dependent signalling. Recent progress made in our understanding of the structure and function of photosensory receptors and their downstream effector molecules is discussed.

Photoregulation of Cellular Morphology during Complementary Chromatic Adaptation Requires Sensor-Kinase-Class Protein RcaE in Fremyella diplosiphon

We used wild-type UTEX481; SF33, a shortened-filament mutant strain that shows normal complementary chromatic adaptation pigmentation responses; and FdBk14, an RcaE-deficient strain that lacks light-dependent pigmentation responses, to investigate the molecular basis of the photoregulation of cellular morphology in the cyanobacterium Fremyella diplosiphon. Detailed microscopic and biochemical analyses indicate that RcaE is required for the photoregulation of cell and filament morphologies of F. diplosiphon in response to red and green light.

Determining cell shape: adaptive regulation of cyanobacterial cellular differentiation and morphology.

Similar to other bacteria, cyanobacteria exist in a wide-ranging diversity of shapes and sizes. However, three general shapes are observed most frequently: spherical, rod and spiral. Bacteria can also grow as filaments of cells. Some filamentous cyanobacteria have differentiated cell types that exhibit distinct morphologies: motile hormogonia, nitrogen-fixing heterocysts, and spore-like akinetes. Cyanobacterial cell shapes, which are largely controlled by the cell wall, can be regulated by developmental and/or environmental cues, although the mechanisms of regulation and the selective advantage(s) of regulating cellular shape are still being elucidated. In this review, recent insights into developmental and environmental regulation of cell shape in cyanobacteria and the relationship(s) of cell shape and differentiation to organismal fitness are discussed.

Root-Localized Phytochrome Chromophore Synthesis Is Required for Photoregulation of Root Elongation and Impacts Root Sensitivity to Jasmonic Acid in Arabidopsis

Plants exhibit organ- and tissue-specific light responses. To explore the molecular basis of spatial-specific phytochrome-regulated responses, a transgenic approach for regulating the synthesis and accumulation of the phytochrome chromophore phytochromobilin (PΦB) was employed. In prior experiments, transgenic expression of the BILIVERDIN REDUCTASE (BVR) gene was used to metabolically inactivate biliverdin IXα, a key precursor in the biosynthesis of PΦB, and thereby render cells accumulating BVR phytochrome deficient. Here, we report analyses of transgenic Arabidopsis (Arabidopsis thaliana) lines with distinct patterns of BVR accumulation dependent upon constitutive or tissue-specific, promoter-driven BVR expression that have resulted in insights on a correlation between root-localized BVR accumulation and photoregulation of root elongation. Plants with BVR accumulation in roots and a PΦB-deficient elongated hypocotyl2 (hy2-1) mutant exhibit roots that are longer than those of wild-type plants under white illumination. Additional analyses of a line with root-specific BVR accumulation generated using a GAL4-dependent bipartite enhancer-trap system confirmed that PΦB or phytochromes localized in roots directly impact light-dependent root elongation under white, blue, and red illumination. Additionally, roots of plants with constitutive plastid-localized or root-specific cytosolic BVR accumulation, as well as phytochrome chromophore-deficient hy1-1 and hy2-1 mutants, exhibit reduced sensitivity to the plant hormone jasmonic acid (JA) in JA-dependent root inhibition assays, similar to the response observed for the JA-insensitive mutants jar1 and myc2. Our analyses of lines with root-localized phytochrome deficiency or root-specific phytochrome depletion have provided novel insights into the roles of root-specific PΦB, or phytochromes themselves, in the photoregulation of root development and root sensitivity to JA.

Detection of Spatial-Specific Phytochrome Responses Using Targeted Expression of Biliverdin Reductase in Arabidopsis

To regulate levels of holophytochrome in a spatial-specific manner and investigate the major sites of action of phytochromes during seedling development, we constructed transgenic Arabidopsis (Arabidopsis thaliana) plant lines expressing plastid-targeted mammalian biliverdin IXα reductase (pBVR) under regulatory control of CAB3 and MERI5 promoters. Comparative photobiological and phenotypic analyses indicated that spatial-specific expression of pBVR led to the disruption of distinct subsets of phytochrome-regulated responses for different promoters. pBVR expression in photosynthetic tissues (CAB3∷pBVR lines) had intermediate effects on chlorophyll accumulation, carotenoid production, anthocyanin synthesis, and leaf development responses in white-light conditions. CAB3∷pBVR expression, however, resulted in distinctive phenotypes in far-red (FR) conditions. A number of FR high irradiance responses were disrupted in CAB∷pBVR lines, including FR-dependent inhibition of hypocotyl elongation and stimulation of anthocyanin accumulation. By contrast, preferential expression of pBVR in the shoot apical meristem in MERI5∷pBVR lines resulted in a phytochrome-deficient, leaf development phenotype under short-day growth conditions. These results implicate leaf-localized phytochrome A as having a unique role in regulating FR-mediated hypocotyl elongation and meristem- and/or leaf primordia-localized phytochromes as having a novel role in phytochrome-dependent responses. Taken together, these studies demonstrate the efficacy of selectively inactivating distinct phytochrome-mediated responses by regulated expression of BVR in transgenic plants, a novel means to investigate the sites of phytochrome photoperception and to regulate specifically light-mediated plant growth and development.

Shedding new light on the regulation of complementary chromatic adaptation

Complementary chromatic adaptation (CCA) is a light-dependent acclimation process that occurs in cyanobacteria and likely is related to increased fitness of these organisms in natural environments. Although CCA has been studied for over 40 years, significant advances in our understanding of the molecular foundations of CCA are still emerging. In this minireview, I explore recently reported developments that include novel insights into the molecular mechanisms utilized in the photoregulation of pigmentation and the molecular basis of light-dependent changes in cellular morphology, which are central elements of the process of CCA. I also discuss future avenues of study that are expected to lead to additional progress in our understanding of CCA and our general appreciation of light sensing and photomorphogenesis in cyanobacteria.

FdTonB is involved in the photoregulation of cellular morphology during complementary chromatic adaptation in Fremyella diplosiphon.

We have characterized a Fremyella diplosiphon TonB protein (FdTonB) and investigated its function during complementary chromatic adaptation. Sequence similarity analysis of FdTonB (571 aa) led to identification of several conserved domains characteristic of TonB proteins, including an N-terminal transmembrane domain, a central proline-rich spacer and a C-terminal TonB-related domain (TBRD). We identified a novel glycine-rich domain containing (Gly-X)(n) repeats. To assess FdTonB function, we constructed a DeltatonB mutant through homologous recombination based upon truncation of the central proline-rich spacer, glycine-rich domain and TBRD. Our DeltatonB mutant exhibited an aberrant cellular morphology under green light, with expanded cell width compared to the parental wild-type (WT) strain. The cellular morphology of the DeltatonB mutant recovered upon WT tonB expression. Interestingly, tonB expression was found to be independent of RcaE. As DeltatonB and WT strains respond in the same way when grown under iron-replete versus iron-limited conditions, our results suggest that FdTonB is not involved in the classic TonB function of mediating cellular adaptation to iron limitation, but exhibits a novel function related to the photoregulation of cellular morphology in F. diplosiphon.

Genome Sequencing of Arabidopsis abp1-5 Reveals Second-Site Mutations That May Affect Phenotypes

Auxin regulates numerous aspects of plant growth and development. For many years, investigating roles for AUXIN BINDING PROTEIN1 (ABP1) in auxin response was impeded by the reported embryo lethality of mutants defective in ABP1. However, identification of a viable Arabidopsis thaliana TILLING mutant defective in the ABP1 auxin binding pocket (abp1-5) allowed inroads into understanding ABP1 function. During our own studies with abp1-5, we observed growth phenotypes segregating independently of the ABP1 lesion, leading us to sequence the genome of the abp1-5 line described previously. We found that the abp1-5 line we sequenced contains over 8000 single nucleotide polymorphisms in addition to the ABP1 mutation and that at least some of these mutations may originate from the Arabidopsis Wassilewskija accession. Furthermore, a phyB null allele in the abp1-5 background is likely causative for the long hypocotyl phenotype previously attributed to disrupted ABP1 function. Our findings complicate the interpretation of abp1-5 phenotypes for which no complementation test was conducted. Our findings on abp1-5 also provide a cautionary tale illustrating the need to use multiple alleles or complementation lines when attributing roles to a gene product.

Right place, right time: Spatiotemporal light regulation of plant growth and development.

Recent advances in our understanding of the roles of photoreceptors in light-dependent regulation of plant growth and development have been rapid and significant. Developments have been reported for numerous plant photoreceptor signaling pathways, yet researchers have made the most progress in increasing our comprehension of the roles of phytochrome family members, as well as the intracellular roles of phytochromes and phytochrome-interacting proteins in light-dependent signaling. An understudied, but vitally important, area of phytochrome biology centers on the roles phytochromes play in intercellular and interorgan signaling at the molecular level that results in the coordination of growth responses between distinct tissues and organs. This frontier of research into spatiotemporal phytochromes, and more generally plant photoreceptors, which is only beginning to be investigated and understood at the molecular genetic level, has a rich history of physiological data.