Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices

Kasprowicz, Anna; Szuba, Agnieszka; Volkmann, Dieter; Baluška, Frantǐsek; Wojtaszek, Przemysław

doi:10.1093/jxb/erp033

Cited by 72 publications

(49 citation statements)

References 76 publications

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“…67,68 The preferential localization and the strong transcriptional responsiveness of both NR and nsHbs in the transition zone of the apex straightened the hypothesis of a role of this root portion in translating the environmental stimuli in developmental response. 67,68 Because of the role of NO in several cytoskeleton-mediated processes in plants, [76][77][78][79][80][81][82][83] the actin-dependent endocytosis and the organization of the actin cytoskeleton are proposed as candidates in transducing the NO-dependent nitrate regulation of root elongation.…”

Section: Nitrate Affects Root Elongation Through No-elicited Actionsmentioning

confidence: 99%

“…Cytoskeletal proteins seem to represent a highly probable molecular target for NO signal [76][77][78] and accumulating evidences place NO among the key elements in the control of a number of cytoskeleton-mediated processes in plants, such as root growth and development, 79 guard cell dynamic, 80 vesicle trafficking, 76 pollen, 81 and root hair tip growth, 82 or gravitropic bending. 83 In particular, Kasprowicz et al 76 demonstrated that the actin-dependent endocytosis and organization of the actin cytoskeleton are modulated by NO levels in maize root apices, according to cell-type and developmental stage with the most remarkable effects noticed at level of the transition zone. Thus, the involvement of cytoskeletal rearrangements in the NO-mediated nitrate regulation of primary root elongation is highly conceivable.…”

Section: Nitrate Affects Root Elongation Through No-elicited Actionsmentioning

confidence: 99%

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NO signaling is a key component of the root growth response to nitrate inZea maysL.

Trevisan

Manoli

Quaggiotti

2014

Plant Signaling & Behavior

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To search for nutrients and water, roots need to efficiently explore large soil volumes. To this aim they generate complex root systems, allowing them to maximize their resource allocation efficiency. 1 Despite the vital importance of roots, the difficulty in accessing intact root systems for analysis, particularly under field conditions, have slowed down the breeding programs for plant's adaptation to environmental restrictions. 2,3 The capacity of plants to take up nutrients and water is mainly determined by changes in the architecture of the root system. 1 Three major processes affect the overall architecture of the root system: the rate of cell division, the rate of cell differentiation, and the extent of expansion and elongation of cells. [4][5][6] Disturbs in any of these 3 processes can affect the whole root-system architecture and the capacity of plants to survive and develop in adverse environments (Giehl et al. 7 and references therein).The root system results from the coordinated control of both genetic endogenous programs (regulating growth and organogenesis) and the action of abiotic and biotic environmental stimuli. 8,9 The dynamic control of the overall root system architecture (RSA) throughout time finally determines root plasticity and allows plants to efficiently adapt to environmental constraints. 10 The soil-environment from which plants extract nutrients and water is extremely heterogeneous, both spatially and temporally. 11 Among the nutrients present in soil, nitrate (NO 3 − ) may vary by an order of magnitude within centimeters or over the course of a day. 12 The effects of NO 3 − on the root system are complex and depend on several factors, such as the concentration available to the plant, the endogenous nitrogen status and the sensitivity of the species. 10,13,14 A considerable part of the studies aimed to unravel the mechanisms controlling RSA growth and development in response to nitrate have been focused on lateral roots (LR), 8,13,[15][16][17][18][19][20] while the nitrate-regulation of the primary root growth is still unclear. Beside NO 3 − , auxin has been demonstrated to strongly affect and control the LR development, [21][22][23][24] and an increasing number of studies suggests an overlap between auxin and NO 3 − signaling pathways in controlling LR development. [25][26][27][28][29][30][31][32][33] NO 3 -has a Doubtful Role in Regulating the Growth of Primary RootsDespite the high amount of reports published on nitrate effects on root elongation, the lack of univocal results makes it difficult to clearly decipher this response ( Table 1). In Arabidopsis thaliana, inhibition of primary root growth has been observed when nitrate is applied homogeneously at high concentrations (50 mM) for 7 d, but not in a range between 0.1 and 10 mM. 35 On the contrary, in this same species Linkohr et al. 36 showed an inhibition of primary root elongation with the increase of nitrate concentration already beyond 0.01 mM, but in this case seedlings were IAA, indole-3-acetic acid; SNP, sodium n...

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Section: Nitrate Affects Root Elongation Through No-elicited Actionsmentioning

confidence: 99%

Section: Nitrate Affects Root Elongation Through No-elicited Actionsmentioning

confidence: 99%

NO signaling is a key component of the root growth response to nitrate inZea maysL.

Trevisan

Manoli

Quaggiotti

2014

Plant Signaling & Behavior

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“…Importantly, it has been shown that nitrosylation of a single Cys residue on mammalian actin can alter actin dynamics in vitro (Dalle-Donne et al, 2000). Moreover, alterations in actin organization have recently been observed in maize (Zea mays) roots treated with the NO donor SNAP (Kasprowicz et al, 2009). …”

Section: Evidence For Ros and No Signaling To Si-induced Actin Foci Imentioning

confidence: 99%

Reactive Oxygen Species and Nitric Oxide Mediate Actin Reorganization and Programmed Cell Death in the Self-Incompatibility Response of Papaver

et al. 2011

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Pollen-pistil interactions are critical early events regulating pollination and fertilization. Self-incompatibility (SI) is an important mechanism to prevent self-fertilization and inbreeding in higher plants. Although data implicate the involvement of reactive oxygen species (ROS) and nitric oxide (NO) in pollen-pistil interactions and the regulation of pollen tube growth, there has been a lack of studies investigating ROS and NO signaling in pollen tubes in response to defined, physiologically relevant stimuli. We have used live-cell imaging to visualize ROS and NO in growing Papaver rhoeas pollen tubes using chloromethyl-2#7#-dichlorodihydrofluorescein diacetate acetyl ester and 4-amino-5-methylamino-2#,7#-difluorofluorescein diacetate and demonstrate that SI induces relatively rapid and transient increases in ROS and NO, with each showing a distinctive "signature" within incompatible pollen tubes. Investigating how these signals integrate with the SI responses, we show that Ca 2+ increases are upstream of ROS and NO. As ROS/NO scavengers alleviated both the formation of SI-induced actin punctate foci and also the activation of a DEVDase/caspase-3-like activity, this demonstrates that ROS and NO act upstream of these key SI markers and suggests that they signal to these SI events. These data represent, to our knowledge, the first steps in understanding ROS/NO signaling triggered by this receptor-ligand interaction in pollen tubes.Pollen-pistil interactions in flowering plants are involved in pivotal events regulating pollination and fertilization. An important mechanism that operates during pollination to prevent inbreeding and its consequential debilitating effects is self-incompatibility (SI). Three distinct SI systems have been identified to date at the molecular level, which suggests that SI has evolved independently several times (for recent reviews, see Takayama and Isogai, 2005;Franklin-Tong, 2008). These systems use a variety of mechanisms to prevent self-fertilization. Despite being controlled by different genes, all the SI systems use an S-locus. Selffertilization is prevented by use of a specific recognition system, which results in "self" pollen (i.e. incompatible pollen) being rejected at some point in the pollination process, while compatible pollen is allowed to grow freely. The S-locus is multiallelic, which allows for different specificities to be generated, and combinations of different haplotypes allow discrimination between self and nonself. When pollen S-and pistil S-haplotypes match, this creates an incompatible combination and incompatible pollen is rejected.

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“…30 Furthermore, the involvement of NO in actin cytoskeleton and vesicle trafficking in root apices has been demonstrated. 31 Thus, the currently available data allowed us to speculate that NO can directly influence the activity of target proteins through S-nitrosylation or acting that cell elongation during post-embryonic hypocotyl and root hair growth are under the control of light-regulated developmental switch. 18 However, it seems that light requirements for phytochrome action may be different for hypocotyl and root hair growth.…”

Section: Linking Signaling Pathways To Gain Understanding On the Regumentioning

confidence: 99%

Extracellular ATP and nitric oxide signaling pathways regulate redox-dependent responses associated to root hair growth in etiolated Arabidopsis seedlings

Terrile

Tonón

Iglesias

et al. 2010

Plant Signaling & Behavior

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Addendum to: Tonón C, Terrile MC, Iglesias MJ, Lamattina L, Casalongué C. Extracellular ATP, nitric oxide and superoxide act coordinately to regulate hypocotyl growth in etiolated Arabidopsis seedlings. J Plant Physiol 2010; 167:540-546; PMID: 19962212; DOI: 10.1016 DOI: 10. /j.jplph.2009. E xtracellular ATP (eATP) and nitric oxide (NO) have emerged as crucial players in plant development, stress responses and cell viability. Glutathione (GSH) is an abundant reducing agent with proposed roles in plant growth, development and stress physiology. In a recent publication, we demonstrated that eATP and NO restore hypocotyl elongation of etiolated Arabidopsis seedlings treated with GSH. Here it is reported that exogenous ATP also restores root hair growth suggesting a role for ATP and NO in the regulation of redox balance associated to specific processes of plant morphogenesis. A tentative model integrating redox-, eATPand NO-signaling pathways during root hair growth in Arabidopsis seedlings is presented. Linking Signaling Pathways to Gain Understanding on the Regulation of Morphological Processes in PlantsThe first living organisms evolved under reducing conditions a long time before the environment became oxidizing due to oxygen produced by photosynthesis. As a consequence, the most fundamental signaling pathways were initially adapted to reducing conditions. Plants, as sessile organisms have taken advantage of the regulatory mechanisms evolved on a changing redox-status and nowadays they are strongly dependent of environmental redox conditions. An efficient redox control together with other signaling mechanisms cooperates to maintain the steady-state redox homeostasis in plant cell. In this scenario, two small signaling molecules such as ATP and NO have a very ancient origin and are involved in cell redox physiology. 1,2 ATP and NO play diverse biological functions in phylogenetically distant species. Intracellular ATP is the major source of energy for cellular reactions. However, ATP also acts as a signaling molecule at the extracellular face of the plasma membrane in animals as well as in plants. 3 NO is an important regulatory molecule in eukaryotes. Several roles have been attributed to extracellular ATP (eATP) and NO in plants, ranging from cell viability to pathogen defence and cell death.2-4 NO production stimulated by eATP was shown in tomato suspension cells, 5 hairy roots of Salvia miltiorrhiza 6 as well as in algae. 7 Reichler et al. 8 showed that the intersection of eATP signaling and NO via the cellular messenger cGMP regulates pollen germination and pollen tube growth in Arabidopsis. Thus, the biochemical and molecular mechanisms underlying eATP and NO signaling pathways in plants have just begun to emerge. Lately, we have described an interconnection between eATP, NO and redox system during hypocotyl elongation in etiolated Arabidopsis seedlings. 9It was demonstrated that a fine-tuning of redox balance and endogenous NO level is associated to eATP action. Therefore, these findings open a new w...

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Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices

Cited by 72 publications

References 76 publications

NO signaling is a key component of the root growth response to nitrate inZea maysL.

NO signaling is a key component of the root growth response to nitrate inZea maysL.

Reactive Oxygen Species and Nitric Oxide Mediate Actin Reorganization and Programmed Cell Death in the Self-Incompatibility Response of Papaver

Extracellular ATP and nitric oxide signaling pathways regulate redox-dependent responses associated to root hair growth in etiolated Arabidopsis seedlings

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