Advances in Plant ER Architecture and Dynamics

Stefano, Giovanni; Brandizzí, Federica

doi:10.1104/pp.17.01261

Cited by 40 publications

(31 citation statements)

References 91 publications

(94 reference statements)

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“…Differential regulation of their cleavage and corresponding kinetics, dependent on the upstream signal, and the specificity for their target genes would allow for a highly combinatorial and fine-tuned response, as is evident from the complex interactions of regulators and DEGs identified by the GRN. This potential is further highlighted by emerging evidence of a direct physical association of the ER with mitochondria and chloroplasts (Stefano and Brandizzi, 2018), allowing for a direct signal transduction through membrane-associated proteins. The positive feedback loops initiated by binding of ANAC017 to the promoter of ANAC013 (Ng et al, 2013), resulting in a large increase in gene expression, reinforces a function of ANAC017 as a master regulator, with ANAC013 and possibly other ANACs as checkpoints, and also involving the UPR.…”

Section: Discussionmentioning

confidence: 99%

ANAC017 Coordinates Organellar Functions and Stress Responses by Reprogramming Retrograde Signaling

Meng

Clercq

et al. 2019

Plant Physiol.

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Mitochondria adjust their activities in response to external and internal stimuli to optimize growth via the mitochondrial retrograde response signaling pathway. The Arabidopsis (Arabidopsis thaliana) NAC domain transcription factor ANAC017 has previously been identified as a regulator of the mitochondrial retrograde response. We show here that overexpression of ANAC017 in Arabidopsis leads to growth retardation, altered leaf development with decreased cell size and viability, and early leaf senescence. RNA sequencing analyses revealed that increased ANAC017 expression leads to higher expression of genes related to mitochondrial stress, cell death/autophagy, and leaf senescence under nonlimiting growth conditions as well as extensive repression of chloroplast function. Gene regulatory network analysis indicated that a complex hierarchy of transcription factors exists downstream of ANAC017. These involve a set of up-regulated ANAC and WRKY transcription factors associated with organellar signaling and senescence. The network also includes a number of ethylene-and gibberellic acid-related transcription factors with established functions in stress responses and growth regulation, which down-regulate their target genes. A number of BASIC LEUCINE-ZIPPER MOTIF transcription factors involved in the endoplasmic reticulum unfolded protein response or balancing of energy homeostasis via the SNF1-RELATED PROTEIN KINASE1 were also down-regulated by ANAC017 overexpression. Our results show that the endoplasmic reticulum membrane tethering of the constitutively expressed ANAC017, and its controlled release, are crucial to fine-tune a fast reactive but potentially harmful signaling cascade. Thus, ANAC017 is a master regulator of cellular responses with mitochondria acting as central sensors.

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Section: Discussionmentioning

confidence: 99%

ANAC017 Coordinates Organellar Functions and Stress Responses by Reprogramming Retrograde Signaling

Meng

Clercq

et al. 2019

Plant Physiol.

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“…The fluorescent protein-tagged CHX23 was localized at reticulate membranes and with ER markers in transfected pollen tubes. The possibility that CHX23-associated ER affects endosome or PM dynamics and function (Bayer et al, 2017;Stefano and Brandizzi, 2018) is considered. One model is that CHX21-and CHX23-mediated cation and pH balance is critical for signal reception or transduction, which includes trafficking via the cytoskeleton and processes that lead to a shift in directional tube growth (Lu et al, 2011).…”

Section: Pollen Tube Signaling and Navigationmentioning

confidence: 99%

Plant Endomembrane Dynamics: Studies of K⁺/H⁺ Antiporters Provide Insights on the Effects of pH and Ion Homeostasis

2018

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Plants remodel their cells through the dynamic endomembrane system. Intracellular pH is important for membrane trafficking, but the determinants of pH homeostasis are poorly defined in plants. Electrogenic proton (H) pumps depend on counter-ion fluxes to establish transmembrane pH gradients at the plasma membrane and endomembranes. Vacuolar-type H-ATPase-mediated acidification of the trans-Golgi network is crucial for secretion and membrane recycling. Pump and counter-ion fluxes are unlikely to fine-tune pH; rather, alkali cation/H antiporters, which can alter pH and/or cation homeostasis locally and transiently, are prime candidates. Plants have a large family of predicted cation/H exchangers (CHX) of obscure function, in addition to the well-studied K(Na)/H exchangers (NHX). Here, we review the regulation of cytosolic and vacuolar pH, highlighting the similarities and distinctions of NHX and CHX members. In planta, alkalinization of the trans-Golgi network or vacuole by NHXs promotes membrane trafficking, endocytosis, cell expansion, and growth. CHXs localize to endomembranes and/or the plasma membrane and contribute to male fertility, pollen tube guidance, pollen wall construction, stomatal opening, and, in soybean (), tolerance to salt stress. Three-dimensional structural models and mutagenesis of Arabidopsis () genes have allowed us to infer that AtCHX17 and AtNHX1 share a global architecture and a translocation core like bacterial Na/H antiporters. Yet, the presence of distinct residues suggests that some CHXs differ from NHXs in pH sensing and electrogenicity. How H pumps, counter-ion fluxes, and cation/H antiporters are linked with signaling and membrane trafficking to remodel membranes and cell walls awaits further investigation.

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“…In plant cells, the ER consists of a dynamic network of cisternae (sheets) and, more predominantly, tubules which extend throughout the cytoplasm and across cellular boundaries, with intimate connections to other organelles such as the Golgi, the plasma membrane, the outer membrane of the nuclear envelope and the cytoskeleton (Goyal & Blackstone, 2013;Hawes et al, 2015;Stefano & Brandizzi, 2017). Hence, the ER is crucial to the maintenance of cellular homeostasis.…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis Lunapark proteins are involved in ER cisternae formation

et al. 2018

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Summary The plant endoplasmic reticulum (ER) is crucial to the maintenance of cellular homeostasis. The ER consists of a dynamic and continuously remodelling network of tubules and cisternae. Several conserved membrane proteins have been implicated in formation and maintenance of the ER network in plants, such as RHD3 and the reticulon proteins. Despite the recent work in mammalian and yeast cells, the detailed molecular mechanisms of ER network organization in plants remain largely unknown. Recently, novel ER network‐shaping proteins called Lunapark (LNP) have been identified in yeast and mammalian cells.Here we identify two Arabidopsis LNP homologues and investigate their subcellular localization via confocal microscopy and potential function in shaping the ER network using protein–protein interaction assays and mutant analysis.We show that AtLNP1 overexpression in tobacco leaf epidermal cells mainly labels cisternae in the ER network, whereas AtLNP2 labels the whole ER. Overexpression of LNP proteins results in an increased abundance of ER cisternae and lnp1 and lnp1lnp2 amiRNA lines display a reduction in cisternae and larger polygonal areas.Thus, we hypothesize that AtLNP1 and AtLNP2 are involved in determining the network morphology of the plant ER, possibly by regulating the formation of ER cisternae.

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Advances in Plant ER Architecture and Dynamics

Cited by 40 publications

References 91 publications

ANAC017 Coordinates Organellar Functions and Stress Responses by Reprogramming Retrograde Signaling

ANAC017 Coordinates Organellar Functions and Stress Responses by Reprogramming Retrograde Signaling

Plant Endomembrane Dynamics: Studies of K⁺/H⁺ Antiporters Provide Insights on the Effects of pH and Ion Homeostasis

Arabidopsis Lunapark proteins are involved in ER cisternae formation

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Advances in Plant ER Architecture and Dynamics

Cited by 40 publications

References 91 publications

ANAC017 Coordinates Organellar Functions and Stress Responses by Reprogramming Retrograde Signaling

ANAC017 Coordinates Organellar Functions and Stress Responses by Reprogramming Retrograde Signaling

Plant Endomembrane Dynamics: Studies of K+/H+ Antiporters Provide Insights on the Effects of pH and Ion Homeostasis

Arabidopsis Lunapark proteins are involved in ER cisternae formation

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Plant Endomembrane Dynamics: Studies of K⁺/H⁺ Antiporters Provide Insights on the Effects of pH and Ion Homeostasis