https://orcid.org/0000-0003-2557-795X
ABSTRACT
Plasma membrane NADPH oxidases (NOXs), also named respiratory burst oxidase homologues (Rbohs), are critical generators of reactive oxygen species (ROS), which as signal molecules regulate growth and development, and adaptation to various biotic and abiotic stresses in plants. NOXs-dependent ROS production is frequently induced by diverse phytohormones. The ROS commonly function downstream of, and interplay with hormone signalings, coordinately modulating plant development and stress tolerance. In this review, we summarize recent advances on the roles and molecular mechanisms of Rbohs in mediating signalings of multiple hormones including auxin, gibberellins, abscisic acid, ethylene and brassinosteroids in plants.
Reactive oxygen species (ROS) such as superoxide anion (O2•−) and hydrogen peroxide (H2O2) are byproducts of cellular metabolisms in plants. They are produced in different organelles or subcellular compartments.Citation1,Citation2 Excessive ROS are harmful for plant growth and survival, and the levels of ROS in cells are efficiently and reversibly balanced by a variety of ROS scavenging systems.Citation1,Citation2 During long-term evolution, plants have utilized ROS as signal molecules to regulate growth and development, and responses to diverse biotic and abiotic environmental stresses.Citation2–Citation5
ROS are synthesized by both enzymatic and non enzymatic reactions in plants. Plasma membrane NADPH oxidases (NOXs), also known as respiratory burst oxidase homologues (Rbohs), are essential producers of ROS. Rbohs transfer electrons from cytoplasmic NAD(P)H to O2 to form O2•−, which rapidly converts to H2O2 spontaneously or catalyzed by superoxide dismutase.Citation6–Citation8 Rbohs have been demonstrated to be vital players of numerous cellular processes such as pathogene defense, stomatal closure, seed germination, root growth, reproductive development, and adaptations to various abiotic stress.Citation6–Citation9 In Arabidopsis genome, 10 Rboh genes (AtRbohA-J) have been identified. AtRbohB serves a role in seed after-ripening.Citation10 AtRbohC positively regulates root hair growth and cellular integrity.Citation11,Citation12 AtrbohD and AtrbohF synergistically or independently function in root formation, stomatal closure, and in responding to diverse stresses.Citation7,Citation8,Citation13–Citation17 AtrbohE is involved in modulating programmed cell death,Citation18 and AtrbohI regulates drought stress response in seeds and roots.Citation19 Both AtrbohH and AtrbohI are key regulators of pollen tube tip growth and polar root hair growth.Citation20,Citation21
NOXs also play pivotal roles in numerous cellular processes regulated by phtohormones.Citation9 NOXs-dependent ROS signals interact with hormone signals, coordinately regulating plant growth and development, and acclimation to diverse environmental stresses. Previously, Xia et al have discussed the crosstalks between NOXs-produced ROS and hormones in plants.Citation9 In this review, we focus on recent work that highlights the roles and mechanisms of Rbohs in mediating hormone signalings in plants.
NOXs exert effects in lateral root formation, polar growth and response to hypoxia modulated by auxin
Auxin is a crucial hormone that controls nearly all aspects of plant growth and development. It can induce the generation of ROS, which in turn regulate auxin signaling as well as auxin-controlled growth programmes.Citation9 Evidence indicated NOXs are critical for lateral root (LR) emergence regulated by auxin.Citation22 It was found that exogenous ROS can rescue the LR-lack phenotype of Arabidopsis double mutant aux1 lax3 (auxin 1, like AUX1 3), in which the auxin influx carrier genes AUX1 and LAX3 are disrupted. AUX1 and LAX3 act in the accumulation of auxin in cortical and epidermal cells overlying new LR primordia (LRPs). The accumulated auxin induces the expression of cell wall remodeling genes, thereby facilitating LR initiation and emergence. ROS play significant roles in auxin-stimulated wall remodeling during LRP development, possibly through wall acidification of the cells overlying LRP.Citation22 Moveover, multiple AtRboh genes (AtRbohA, AtRbohC, AtRbohD and AtRbohE) are active in the cells related to LR emergence. Mutants of AtRbohC, AtRbohD and/or AtRbohE showed delayed LR development. Auxin also induces the spatial expression of several AtRbohs including AtRbohA, AtRbohC, AtRbohD, AtRbohE, AtRbohF, AtRbohG and AtRbohI in roots.Citation22 Collectively, these results suggest auxin signalings regulate the expression of AtRbohs, and subsequent production of ROS in roots, promoting LR outgrowth in Arabidopsis.
NOXs are responsible for auxin-modulated root hair growth. Mangano et al observed that auxin-controlled auxin response factor (ARF) like ARF5, ARF7, ARF8 and ARF19 transcriptionally activate the bHLH transcription factor RSL4 (Root hair defective six-like 4), which up-regulates the expression of genes encoding AtrbohC, AtrbohJ and AtrbohH, as well as class III peroxidases.Citation21 The NOXs and peroxidase catalyze the synthesis of ROS, further promoting root hair cell elongation.Citation21
NOXs also modulate auxin signal transduction under oxygen deficiency in Arabidopsis.Citation23 Under submergence condition, mutants of AtrbohI shows clearly decreased survival rate and chlorophyll contents, and reduced expression levels of hypoxia responsive genes including AtHRE1 (Hypoxia responsive ethylene-responsive transcription factor 1), AtADH1 (Alcohol dehydrogenase 1), AtLDH (Lactate dehydrogenase), and AtSUS1 (Sucrose synthase 1). Oxygen deprivation substantially increases the expression of AtrbohI. The increased effects are markedly inhibited by auxin transport inhibitor 1-naphthylphthalamic acid (NPA). Moreover, lack of auxin causes the reduction of the transcriptional abundances of AtSUS1 in AtrbohI mutants. Disruption of AtrbohI lowers the increases in the expression of auxin-responsive genes induced by oxygen starvation,Citation23 indicating that AtrbohI is involved in auxin signaling under oxygen deprivation. Auxin regulates hypoxia response likely through affecting ethylene biosynthesis under hypoxia in Arabidopsis.Citation23
NOXs positively regulate gibberellins-induced seed germination
Gibberellins (GAs) serve vital roles in modulating many aspects of plant growth and development including activating α-amylase in aleurone cells and promoting seed germination.Citation24 ROS has been demonstrated to positively influence seed germination, and NOXs are an important player during the process.Citation25 During barley seed germination, NOX genes are highly expressed in embryotic cells, and a large amount of NOXs-dependent ROS are generated, which stimulate GA biosynthesis in embryos through increasing the expression of HvGA20ox1 (GA20-oxidase 1), HvGA3ox1, HvGA2ox4 and HvKAO1 (Ent-kaurenoic acid oxidase 1), key genes involved in GA synthesis. NOXs also positively regulate α-amylase activities induced by GA in embryotic cells. The combined effects of NOXs significantly promote seed germination in barley.Citation25,Citation26 Additionally, NOXs activity in aleurone cells enhances after treatment with GA. GA most likely induces the enhancement of Ca2+ in aleurone cells, further activating NOXs in barley seed germination.Citation25
NOXs promote seed germination through degradation of ABA
ABA plays pivotal roles in plant responses to various biotic and abiotic stresses, as well as in regulating stomatal closure, and growth and development.Citation27,Citation28 Evidence reveals that NOXs function in barley seed germination via affecting ABA catabolism.Citation25 During barley seed germination, NOXs inhibitor DPI (Diphenylene iodonium) clearly decreases endogenous ABA levels in embryos, and suppresses the expression of HvABA8′OH-1 (ABA8′-hydroxylase-1), a gene required for ABA catabolism. This indicates that NOXs may stimulate ABA catabolism through impacting the expression of HvABA8′OH-1, further inducing seed germination. ABA also inhibits the expression of HvRbohB1, HvRbohE, HvRbohF1 and HvRbohF2, and activity of NOXs and ROS production in embryos of barley.Citation25
NOXs play roles in scald development and response to abiotic stresses regulated by ethylene
Ethylene is involved in regulating plant growth including cell expansion and fruit ripening, senescence, and multiple stress responses.Citation29 It also acts in apple scald development after exposure to cold stress. Zermiani et al investigated the action and mechanisms of ethylene regulating the scald formation in apple fruit superficies in response to cold stress, and found that ethylene negatively modulates the ROP-GAP rheostat, and progressively impairs apoplastic H2O2 homeostasis, further promoting the scald development.Citation30 NOXs, as key components of ROP-GAP rheostat, are essential for maintainance of the ROS equilibrium. Ethylene downregulates the expression of MdRbohF and particularly MdRbohC, leading to the disturbance of the apple ROP-GAP rheostat machinery and ‘ROS gene network’, thereby disruption of apoplastic ROS homeostasis during cold exposure.Citation30
Rbohs also function in AtERF73 (Ethylene-responsive factors73)/HRE1-mediated feedback regulation of hypoxia signaling in Arabidopsis.Citation31 AtERF73/HRE1 is a central regulator of ethylene responses under hypoxia.Citation32 It is also regulated by ROS, the key components of oxygen deficiency signaling. Under oxygen starvation, NOXs-dependent ROS are rapidly generated, which affect ethylene signaling, and trigger downstream transcriptional responses of hypoxia-inducible genes including AtERF73/HRE1.Citation32,Citation33 Recently, Yang et al found that hypoxia-induced production of H2O2 in mutants of AtERF73/HRE1 significantly reduces.Citation31 Moreover, the expression of AtRbohB and AtRbohD clearly enhances while that of AtRbohG decreases in AtERF73/HRE1 mutants. The transcriptional abundances of AtRbohI also markedly alter in the AtERF73/HRE1 mutants.Citation31 These results imply that AtERF73/HRE1 regulates H2O2 generation through impacting the hypoxia-stimulated expression of many AtRboh genes under oxygen deficiency.
Studied showed that NOXs have effects in ethylene-induced aerenchyma formation under oxygen limited conditions.Citation34 In rice, the expression of OsRbohH is highly induced in root cortical cells. Mutation of OsRbohH or inhibition of NOX activity significantly suppresses ROS production and ethylene-stimulated aerenchyma formation. OsRbohH is activated by CDPK5 (Calcium-dependent protein kinase 5) and CDPK13 in N. benthamiana leaves, and Ca2+ signaling is involved in aerenchyma formation in rice roots.Citation34 These results demonstrated that CDPK5- and/or CDPK13-mediated Ca2+ stimulates OsRbohH-dependent ROS generation, further promoting ethylene-induced aerenchyma formation in rice roots under hypoxia.
Similarly in sunflower, ROS showed to mediate ethylene-induced aerenchyma formation in stem. In addition, pretreatment with DPI partially inhibits the aerenchyma formation modulated by ethylene,Citation35 pointing to the importance of NOXs in ethylene signaling. Yet, which NOX subunits play a role in the processes is unexplored.
Additionally, NOXs are responsible for the resistance to multiple abiotic stresses controlled by ERF74.Citation36 ERF74 positively regulates Arabidopsis tolerance to drought, high light, heat and aluminum stresses through inducing ROS burst in the early stages of various stresses. The ROS burst relys on the high expression of AtRbohD. ERF74 directly binds to the GCC cis-elements of AtRbohD promoter and activates its expression under the abiotic stresses. Also, AtRbohD-dependent ROS burst is required for inducing the expression of many stress marker genes involving in flooding, drought and aluminum stress, and in ROS scavenging enzyme genes under different stresses in Arabidopsis.Citation36
NOXs function in brassinosteroids-mediated stomatal closure, systemic resistance and seedling growth
Brassinosteroids (BRs) are key growth promoting hormones. They modulate cell division, elongation and vascular differentiation, and stress response.Citation37 BRs positively and negatively affect ABA-induced stomatal closure.Citation38 BR mutant bri1-301 shows decreased sensitivity to ABA-promoted stomatal closure, suggesting BR signaling is required for ABA modulated stomatal closure. However, high levels of BR suppress ABA-evoked stomatal closure. Further studies revealed that BR inhibits the enhancements in expression of AtrbohD, AtrbohF, AtNIA1 (Nitrate reductase 1) and ATNIA2 elicited by ABA, thereby repressing ABA promotion of ROS production and nitric oxide (NO) synthesis.Citation38 This suggests that BR suppresses ABA-mediated stomatal closure at least partially through inhibiting ABA-induced expression of AtrbohD and AtrbohF.
NOXs also essential for BR-induced systemic virus resistance in Nicotiana benthamiana.Citation39 BR has shown to trigger system resistance to virus, and the accumulation of ROS and NO in leave of Nicotiana benthamiana. The ROS are originated from NOXs, particularly NbRbohB because silencing of the gene NbRbohB notably suppresses BRs-stimulated ROS production and systemic immunity response. Moreover, in the presence of BRs, NbRbohB-mediated ROS accumulation is regulated by BR receptor kinase NbBRI1 (BR insensitive 1).Citation39
Recently, Song et al observed that the reduction in BR levels or deficiency of BR receptor promotes the sensitivity of tomato plants to the nematode Meloidogyne incognita while application of BR has the opposite effects.Citation40 Further study reveals that lack of BR leads to marked decreases in apoplastic ROS generation and the expression levels of Rboh1, and the activation of mitogen-activated protein kinase 1/2 (MPK1/2) and MPK3 in roots. Compared with the wild-type plants, the silenced lines of Rboh1, MPK1, MPK2 and MPK3 genes showed elevated susceptibility of roots to nematode infection, and arrested resistance against the nematode triggered by BR. These results indicate that the Rbohs-mediated the activation of MPK cascade plays significant roles in BR-induced systemic resistance against the nematode in tomato.
NOXs have been demonstrated to mediate BR controlled Arabidopsis seedling development (including hypocotyls elongation and root meristem development), Tian et al reported that H2O2 stimulates the oxidation of the key BR signaling transcription factor BZR1 (Brassinazole-resistant 1), further increasing the transcriptional activity of BZR1 by promoting its interaction with the crucial auxin-signaling regulator ARF6 (Auxin response factor 6) and the key light-signaling regulator PIF4 (Phytochrome interacting factor 4), thereby facilitating seedling growth.Citation41 DPI significantly represses BR-induced H2O2 generation and BR-promoted hypocotyl elongation and cell division of root quiescent center (QC). Moreover, double mutant atrbohd/atrbohf is hyposensitive to BR-modulated hypocotyl elongation and QC cell division,Citation41 highlighting the great importance of AtrbohD and AtrbohF in BR regulated growth and development.
In summary, recent evidence reveals that NOXs play crucial roles in the multiple hormone signalings. However, the molecular mechanisms for most hormones activating NOXs during growth or under some specific stresses are largely unknown. The regulation mechanisms for NOXs mediating hormone signalings in many cases also remain to be thoroughly investigated in the future.
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References
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