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Auxin/Cytokinin Antagonistic Control of the Shoot/Root Growth Ratio and Its Relevance for Adaptation to Drought and Nutrient Deficiency Stresses.
Kurepa, J, Smalle, JA
International journal of molecular sciences. 2022;(4)
Abstract
The hormones auxin and cytokinin regulate numerous aspects of plant development and often act as an antagonistic hormone pair. One of the more striking examples of the auxin/cytokinin antagonism involves regulation of the shoot/root growth ratio in which cytokinin promotes shoot and inhibits root growth, whereas auxin does the opposite. Control of the shoot/root growth ratio is essential for the survival of terrestrial plants because it allows growth adaptations to water and mineral nutrient availability in the soil. Because a decrease in shoot growth combined with an increase in root growth leads to survival under drought stress and nutrient limiting conditions, it was not surprising to find that auxin promotes, while cytokinin reduces, drought stress tolerance and nutrient uptake. Recent data show that drought stress and nutrient availability also alter the cytokinin and auxin signaling and biosynthesis pathways and that this stress-induced regulation affects cytokinin and auxin in the opposite manner. These antagonistic effects of cytokinin and auxin suggested that each hormone directly and negatively regulates biosynthesis or signaling of the other. However, a growing body of evidence supports unidirectional regulation, with auxin emerging as the primary regulatory component. This master regulatory role of auxin may not come as a surprise when viewed from an evolutionary perspective.
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Auxin biosynthesis maintains embryo identity and growth during BABY BOOM-induced somatic embryogenesis.
Li, M, Wrobel-Marek, J, Heidmann, I, Horstman, A, Chen, B, Reis, R, Angenent, GC, Boutilier, K
Plant physiology. 2022;(2):1095-1110
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Abstract
Somatic embryogenesis is a type of plant cell totipotency where embryos develop from nonreproductive (vegetative) cells without fertilization. Somatic embryogenesis can be induced in vitro by auxins, and by ectopic expression of embryo-expressed transcription factors like the BABY BOOM (BBM) AINTEGUMENTA-LIKE APETALA2/ETHYLENE RESPONSE FACTOR domain protein. These different pathways are thought to converge to promote auxin response and biosynthesis, but the specific roles of the endogenous auxin pathway in somatic embryogenesis induction have not been well-characterized. Here we show that BBM transcriptionally regulates the YUCCA3 (YUC3) and YUC8 auxin biosynthesis genes during BBM-mediated somatic embryogenesis in Arabidopsis (Arabidopsis thaliana) seedlings. BBM induced local and ectopic YUC3 and YUC8 expression in seedlings, which coincided with increased DR5 auxin response and indole-3-acetic acid (IAA) biosynthesis and with ectopic expression of the WOX2 embryo reporter. YUC-driven auxin biosynthesis was required for BBM-mediated somatic embryogenesis, as the number of embryogenic explants was reduced by ca. 50% in yuc3 yuc8 mutants and abolished after chemical inhibition of YUC enzyme activity. However, a detailed YUC inhibitor time-course study revealed that YUC-dependent IAA biosynthesis is not required for the re-initiation of totipotent cell identity in seedlings. Rather, YUC enzymes are required later in somatic embryo development for the maintenance of embryo identity and growth. This study resolves a long-standing question about the role of endogenous auxin biosynthesis in transcription factor-mediated somatic embryogenesis and also provides an experimental framework for understanding the role of endogenous auxin biosynthesis in other in planta and in vitro embryogenesis systems.
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Spatiotemporal auxin distribution in Arabidopsis tissues is regulated by anabolic and catabolic reactions under long-term ammonium stress.
Dziewit, K, Pěnčík, A, Dobrzyńska, K, Novák, O, Szal, B, Podgórska, A
BMC plant biology. 2021;(1):602
Abstract
BACKGROUND The plant hormone auxin is a major coordinator of plant growth and development in response to diverse environmental signals, including nutritional conditions. Sole ammonium (NH4+) nutrition is one of the unique growth-suppressing conditions for plants. Therefore, the quest to understand NH4+-mediated developmental defects led us to analyze auxin metabolism. RESULTS Indole-3-acetic acid (IAA), the most predominant natural auxin, accumulates in the leaves and roots of mature Arabidopsis thaliana plants grown on NH4+, but not in the root tips. We found changes at the expressional level in reactions leading to IAA biosynthesis and deactivation in different tissues. Finally, NH4+ nutrition would facilitate the formation of inactive oxidized IAA as the final product. CONCLUSIONS NH4+-mediated accelerated auxin turnover rates implicate transient and local IAA peaks. A noticeable auxin pattern in tissues correlates with the developmental adaptations of the short and highly branched root system of NH4+-grown plants. Therefore, the spatiotemporal distribution of auxin might be a root-shaping signal specific to adjust to NH4+-stress conditions.
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No Time for Transcription-Rapid Auxin Responses in Plants.
Dubey, SM, Serre, NBC, Oulehlová, D, Vittal, P, Fendrych, M
Cold Spring Harbor perspectives in biology. 2021;(8)
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Abstract
Auxin regulates the transcription of auxin-responsive genes by the TIR1/AFBs-Aux/IAA-ARF signaling pathway, and in this way facilitates plant growth and development. However, rapid, nontranscriptional responses to auxin that cannot be explained by this pathway have been reported. In this review, we focus on several examples of rapid auxin responses: (1) the triggering of changes in plasma membrane potential in various plant species and tissues, (2) inhibition of root growth, which also correlates with membrane potential changes, cytosolic Ca2+ spikes, and a rise of apoplastic pH, (3) the influence on endomembrane trafficking of PIN proteins and other membrane cargoes, and (4) activation of ROPs (Rho of plants) and their downstream effectors such as the cytoskeleton or vesicle trafficking. In most cases, the signaling pathway triggering the response is poorly understood. A role for the TIR1/AFBs in rapid root growth regulation is emerging, as well as the involvement of transmembrane kinases (TMKs) in the activation of ROPs. We discuss similarities and differences among these rapid responses and focus on their physiological significance, which remains an enigma in most cases.
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5.
Light participates in the auxin-dependent regulation of plant growth.
Lv, B, Zhu, J, Kong, X, Ding, Z
Journal of integrative plant biology. 2021;(5):819-822
Abstract
Light is the energy source for plant photosynthesis and influences plant growth and development. Through multiple photoreceptors, plant interprets light signals through various downstream phytohormones such as auxin. Recently, Chen et al. (2020) uncover a new layer of regulation in IPyA pathway of auxin biosynthesis by light. Here we highlight recent studies about how light controls plant growth through regulating auxin biosynthesis and signaling.
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6.
Auxin-Regulated Lateral Root Organogenesis.
Cavallari, N, Artner, C, Benkova, E
Cold Spring Harbor perspectives in biology. 2021;(7)
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Abstract
Plant fitness is largely dependent on the root, the underground organ, which, besides its anchoring function, supplies the plant body with water and all nutrients necessary for growth and development. To exploit the soil effectively, roots must constantly integrate environmental signals and react through adjustment of growth and development. Important components of the root management strategy involve a rapid modulation of the root growth kinetics and growth direction, as well as an increase of the root system radius through formation of lateral roots (LRs). At the molecular level, such a fascinating growth and developmental flexibility of root organ requires regulatory networks that guarantee stability of the developmental program but also allows integration of various environmental inputs. The plant hormone auxin is one of the principal endogenous regulators of root system architecture by controlling primary root growth and formation of LR. In this review, we discuss recent progress in understanding molecular networks where auxin is one of the main players shaping the root system and acting as mediator between endogenous cues and environmental factors.
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Molecular mechanisms and hormonal regulation underpinning morphological dormancy: a case study using Apium graveolens (Apiaceae).
Walker, M, Pérez, M, Steinbrecher, T, Gawthrop, F, Pavlović, I, Novák, O, Tarkowská, D, Strnad, M, Marone, F, Nakabayashi, K, et al
The Plant journal : for cell and molecular biology. 2021;(4):1020-1036
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Abstract
Underdeveloped (small) embryos embedded in abundant endosperm tissue, and thus having morphological dormancy (MD) or morphophysiological dormancy (MPD), are considered to be the ancestral state in seed dormancy evolution. This trait is retained in the Apiaceae family, which provides excellent model systems for investigating the underpinning mechanisms. We investigated Apium graveolens (celery) MD by combined innovative imaging and embryo growth assays with the quantification of hormone metabolism, as well as the analysis of hormone and cell-wall related gene expression. The integrated experimental results demonstrated that embryo growth occurred inside imbibed celery fruits in association with endosperm degradation, and that a critical embryo size was required for radicle emergence. The regulation of these processes depends on gene expression leading to gibberellin and indole-3-acetic acid (IAA) production by the embryo and on crosstalk between the fruit compartments. ABA degradation associated with distinct spatiotemporal patterns in ABA sensitivity control embryo growth, endosperm breakdown and radicle emergence. This complex interaction between gibberellins, IAA and ABA metabolism, and changes in the tissue-specific sensitivities to these hormones is distinct from non-MD seeds. We conclude that the embryo growth to reach the critical size and the associated endosperm breakdown inside MD fruits constitute a unique germination programme.
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Expansion and innovation in auxin signaling: where do we grow from here?
Ramos Báez, R, Nemhauser, JL
Development (Cambridge, England). 2021;(5)
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Abstract
The phytohormone auxin plays a role in almost all growth and developmental responses. The primary mechanism of auxin action involves the regulation of transcription via a core signaling pathway comprising proteins belonging to three classes: receptors, co-receptor/co-repressors and transcription factors. Recent studies have revealed that auxin signaling can be traced back at least as far as the transition to land. Moreover, studies in flowering plants have highlighted how expansion of the gene families encoding auxin components is tied to functional diversification. As we review here, these studies paint a picture of auxin signaling evolution as a driver of innovation.
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AFB1 controls rapid auxin signalling through membrane depolarization in Arabidopsis thaliana root.
Serre, NBC, Kralík, D, Yun, P, Slouka, Z, Shabala, S, Fendrych, M
Nature plants. 2021;(9):1229-1238
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Abstract
The membrane potential reflects the difference between cytoplasmic and apoplastic electrical potentials and is essential for cellular operation. The application of the phytohormone auxin (3-indoleacetic acid (IAA)) causes instantaneous membrane depolarization in various cell types1-6, making depolarization a hallmark of IAA-induced rapid responses. In root hairs, depolarization requires functional IAA transport and TIR1-AFB signalling5, but its physiological importance is not understood. Specifically in roots, auxin triggers rapid growth inhibition7-9 (RGI), a process required for gravitropic bending. RGI is initiated by the TIR1-AFB co-receptors, with the AFB1 paralogue playing a crucial role10,11. The nature of the underlying rapid signalling is unknown, as well as the molecular machinery executing it. Even though the growth and depolarization responses to auxin show remarkable similarities, the importance of membrane depolarization for root growth inhibition and gravitropism is unclear. Here, by combining the DISBAC2(3) voltage sensor with microfluidics and vertical-stage microscopy, we show that rapid auxin-induced membrane depolarization tightly correlates with RGI. Rapid depolarization and RGI require the AFB1 auxin co-receptor. Finally, AFB1 is essential for the rapid formation of the membrane depolarization gradient across the gravistimulated root. These results clarify the role of AFB1 as the central receptor for rapid auxin responses.
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Manipulation of auxin signalling by plant viruses.
Müllender, M, Varrelmann, M, Savenkov, EI, Liebe, S
Molecular plant pathology. 2021;(11):1449-1458
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Abstract
Compatible plant-virus interactions result in dramatic changes of the plant transcriptome and morphogenesis, and are often associated with rapid alterations in plant hormone homeostasis and signalling. Auxin controls many aspects of plant organogenesis, development, and growth; therefore, plants can rapidly perceive and respond to changes in the cellular auxin levels. Auxin signalling is a tightly controlled process and, hence, is highly vulnerable to changes in the mRNA and protein levels of its components. There are several core nuclear components of auxin signalling. In the nucleus, the interaction of auxin response factors (ARFs) and auxin/indole acetic acid (Aux/IAA) proteins is essential for the control of auxin-regulated pathways. Aux/IAA proteins are negative regulators, whereas ARFs are positive regulators of the auxin response. The interplay between both is essential for the transcriptional regulation of auxin-responsive genes, which primarily regulate developmental processes but also modulate the plant immune system. Recent studies suggest that plant viruses belonging to different families have developed various strategies to disrupt auxin signalling, namely by (a) changing the subcellular localization of Aux/IAAs, (b) preventing degradation of Aux/IAAs by stabilization, or (c) inhibiting the transcriptional activity of ARFs. These interactions perturb auxin signalling and experimental evidence from various studies highlights their importance for virus replication, systemic movement, interaction with vectors for efficient transmission, and symptom development. In this microreview, we summarize and discuss the current knowledge on the interaction of plant viruses with auxin signalling components of their hosts.