How is seed germination regulated in plants

The knowledge gained from such studies will also help to establish a solid foundation to develop future crop improvement strategies. Overall growth and different developmental stages of plants are under strict regulation by several classes of plant hormones. Hormone molecules are present at low concentrations in plants, and they function either at the sites of synthesis or after they are transported to different tissues Santner et al.

In the last two decades, there has been rapid progress in the understanding of the biosynthetic pathways, transport, signaling and mode of action of various plant hormones. Studies related to hormone signaling have established the fact that besides acting on their own, various plant hormones interact in a highly intricate manner Stamm et al.

These findings clearly indicate that plants maintain the availability and level of hormones in different parts of the plant body at different developmental stages in an intricate and balanced manner. A convenient step for us to study plant growth may begin with seed germination.

Successful germination depends on the ability of the plant embryo to gain its metabolic activity Rajjou et al.

Several molecular cues have been revealed by different genetic and proteomic investigations of various Arabidopsis mutants, showing distinct germination-related phenotypes Achard et al. Germination has been found to be under strict regulation of plant hormones, including gibberellic acid GA , abscisic acid ABA , auxin and ethylene Han and Yang, Germination is also significantly affected by several environmental factors, such as various abiotic stresses Rajjou et al.

The constantly changing external factors that most affect plant growth and development are abiotic stresses. Highly variable abiotic stresses affecting plant growth are salinity, drought, and cold. Plants exhibit a range of tolerance levels toward these stresses that are ultimately regulated by complex signaling pathways. Abiotic stresses trigger ABA biosynthesis, which mediates stress adaptive responses by activating several specific signaling cascades and regulating different physiological and growth-related processes.

In the past decade, several genetic, molecular and proteomic studies related to germination and abiotic stresses have been carried out. In this review, we discuss the roles of GA and ABA independently and with the possible crosstalk of these two phytohormones with respect to seed germination and abiotic stresses in various plant species, including crop plants.

Plants are capable of maintaining their internal environment fairly stable within the desired range. Two important factors that are crucial for the maintenance of such homeostasis are internal water level and osmotic state, which are mainly regulated by ABA Zhang et al. ABA acts as a molecular signal in response to various abiotic stresses, which alter the two important physiological functions mentioned above.

These abiotic stress responsive signals are the basis of the various physiological as well as growth-related processes of plants, culminating in their unique ranges of tolerance toward these stresses Finkelstein et al.

ABA which is reported in both primitive and higher organisms seems to have different biosynthesis pathways. In primitive organisms ABA biosynthesis is not well characterized, however, in plant-associated fungi, ABA is reported to be synthesized by the direct cytosolic pathway.

In contrast, great progress has been made in identifying and characterizing the genes involved in ABA metabolism in land plants Hauser et al. ABA biosynthesis in plants follows the organelle-specific indirect pathway.

Further, zeaxanthin is converted to xanthoxin by the enzymatic reaction catalyzed by ZEP enzyme zeaxanthin epoxide and 9- cis -epoxy carotenoid dioxygenase NCED enzyme Hauser et al. Additionally, in crop plants improved tolerance toward various abiotic stresses has been reported by introducing or inducing expression of genes encoding key enzymes of ABA biosynthesis Table 1.

Table 1. Summary of regulation of ABA metabolism and signaling genes with respect to abiotic stress and seed germination in different plant species. The expression of ABA biosynthesis genes is reported to show a direct impact on seed germination along with abiotic stresses. The identification and characterization of NCED genes revealed that the tissue-specific expression of these genes and the resultant modulation of endogenous ABA level at different developmental stages are responsible for the regulation of specific processes, such as seed maturation and seed germination, besides response to abiotic stresses Lefebvre et al.

These and similar findings have clearly established a causal role for ABA in regulating the physiological and developmental processes studied. It is known that ABA accumulates under specific conditions, such as abiotic stresses.

Therefore, the endogenous concentration of biologically active ABA at the site of perception has to be regulated. Apart from biosynthesis, ABA catabolism and transport are the two key essential processes that control ABA-mediated stress regulation.

Several transporters have been identified in different species of plants, which regulate the accumulation and translocation of active ABA along the plant body involving different organelles Kang et al. Also, several genes related to ABA metabolism and transport in different plant species are reported to alter abiotic stress tolerance summarized in Table 1.

Expression profile study of these receptors revealed their role in ABA signaling as well as in the regulation of abiotic stresses Park et al. Triple and quadruple mutants of pyl showed altered ABA sensitivity with respect to seed germination and growth, while overexpression lines conferred tolerance toward abiotic stress Santiago et al.

Their expressions were induced in the presence of ABA. Table 1 summarizes the effect of the genes related to ABA signaling with respect to various abiotic stresses in different plant species. The discovery of bioactive gibberellic acid GA was the result of an investigation of fungal Gibberella fujikuroi infection in rice by Teijiro Yabuta and co-workers Yabuta and Sumiki, Since then, more than a hundred GAs have been identified from different sources, from bacteria to plants.

However, only a few of them have been shown to have biological activity Yamaguchi, ; Hedden and Thomas, Several GA biosynthesis genes are expressed in growing tissues during Arabidopsis development Silverstone et al.

This suggests that biologically active GAs are synthesized at the site of their action in several cases. However, in rice, it has been shown that GA biosynthesis genes are not expressed in the aleurone layer, but GA signaling event occurs there, which suggests paracrine signaling by GAs Kaneko et al.

In addition, in Arabidopsis , GA-dependent gene expressions have been shown in the sites where bioactive GAs are not produced Yamaguchi et al. It has also been shown that early and late steps of GA biosynthesis take place in provascular tissue and, cortex and endodermis, respectively Yamaguchi and Kamiya, ; Yamaguchi et al.

Lack or absence of GA leads to altered GA signaling and germination related phenotype, which has been revealed by different studies done in mutants of GA metabolism Table 2. The relationship between expressions of GA metabolism-related genes and tolerance toward abiotic stresses have been shown. Table 2. Summary of regulation of GA metabolism and signaling genes with respect to abiotic stress and seed germination in different plant species. Characterization of mutants and genetic studies revealed several GA signaling components Hedden and Phillips, ; Stamm et al.

DELLA proteins restrict cell proliferation and expansion by negatively regulating gibberellin signaling and hence inhibit the plant growth Peng et al. The GA signaling components are reported to affect various aspects of germination and abiotic stresses as well Table 2.

DELLAs are also reported to confer salt tolerance in Arabidopsis by altering the duration of vegetative growth. Figure 1. ABA is catabolized to form phaseic acid. ABA transport occurs through different transporters, and ABA elicits distinct signaling cascades in the nucleus and cytoplasm bottom left. GA biosynthesis starts from GGDP in the plastid and a portion of it is catabolized to inactive forms top right. The two signaling pathways crosstalk to regulate seed germination and abiotic stresses bottom right.

Hormones regulate plant growth and development either synergistically or antagonistically, involving a series of complex pathways and networks Liu et al. In the preceding sections, we described the individual roles of GA and ABA in two important aspects affecting plant development; germination and abiotic stresses.

The information summarized in Tables 1 , 2 along with the preceding description show that ABA and GA antagonistically mediate plant developmental processes including seed dormancy and germination. Hence, it is essential to maintain an optimal balance between the endogenous levels of ABA and GA for plant development.

In response to different developmental stages and environmental conditions, various changes occur in the metabolism and signal transductions of these two plant hormones which keep a correct balance between GA and ABA and hence plant homeostasis. In the following sections we will summarize how genes, components and network involving crosstalk of GA and ABA participate in the regulatory processes. In many instances, possible crosstalk events have been shown between ABA and GA with respect to various abiotic stresses and plant growth.

Unfavorable conditions lead to high ABA and low GA levels in seeds whereas favorable conditions cause the reverse situation. Seed dormancy is maintained by ABA whose level is found to progressively increase from embryogenesis to embryo maturation Karssen et al.

ABA restricts embryo growth potential by inhibiting water uptake imbibition and hence cell-wall loosening, which is a key step to start germination Schopfer and Plachy, ; Gimeno-Gilles et al. Under favorable conditions light, temperature and moisture GA biosynthesis and associated pathways are activated, which results in the release from the inhibitory effect of ABA.

Thus, it is clear that various interactions between ABA and GA in seeds help to regulate dormancy and germination. Several recent studies showed the regulation of GA and ABA in light- and temperature-mediated seed germination and dormancy. It indirectly regulates GA biosynthesis genes and directly regulates GA signaling genes. Expression patterns of genes regulating GA and ABA metabolism have been reported to be well coordinated with seasonal seed dormancy in Arabidopsis. Thus, upregulation of GA catabolism and ABA biosynthesis genes was observed during low temperature winter which leads to increased dormancy Footitt et al.

Consistent with that, upregulation of GA biosynthesis ABA catabolism genes have been reported during high temperature spring and summer and decreased dormancy Footitt et al. The transcription factor SPT controls the germination response to cold and light. Various abiotic stresses external environment lead to changes in the plant response and therefore alter the balance of endogenous levels of GA and ABA. This represents another example of how DELLA proteins can control plant growth and abiotic stress tolerance through specific crosstalk with ABA signaling pathway.

Figure 2. Switch from seed dormancy to germination is controlled by the intricate balance between ABA and GA levels. ABA- and GA-signaling and metabolism genes regulate the expression of various genes as mentioned in the text and hence control two of the major aspects of plant development, germination and response to abiotic stresses.

Loss-of-function of these genes leads to the alteration of embryonic leaves cotyledons to take on the appearance of vegetative leaves Gazzarrini et al. These examples clearly show the crosstalk between ABA and GA in controlling seed development as well as germination. Such crosstalk has been predicted based on earlier studies.

With the limited number of definitive studies on such signal crosstalk, we are just beginning to gain valuable insights regarding the regulation of specific growth and developmental processes. It is evident from the foregoing review that the signaling interactions among several phytohormones are common in regulating various stages and processes of plant development. Such regulatory crosstalk can occur at multiple stages of biosynthesis or signaling for different hormones.

Selected genes that play significant roles in the regulation of seed dormancy and germination and various abiotic stresses were also discussed.

It is evident that several positive and negative regulators of ABA and GA have direct or indirect impacts on germination and abiotic stresses. Many transcription factors and signaling components of these two phytohormones help to maintain an intricate balance between endogenous levels of bioactive ABA and GA. Furthermore, studies have identified several ABA and GA crosstalk points showing positive and negative regulation of different molecular modules associated with their metabolism and signaling.

There are a few open questions that can help in formulating the future research directions. Moreover, very few reports on the transport mechanism of GA are available. The antagonistic roles of GA and ABA in controlling developmental processes have been established by several pieces of evidence; however, there could be synergistic crosstalk between GA and ABA in some instances whose underlying molecular mechanisms remain undiscovered.

Although several target genes of a few TFs have been established eg. However, the mechanisms by which these epigenetic regulators mediate crosstalk between GA and ABA need to be investigated. It is known that complexes of TFs regulate downstream target genes Kepka et al. Although several signaling components controlling various aspects of germination and abiotic stresses have been identified, the nature of the underlying mechanisms of many of the events remain to be clarified. Nevertheless, such specific interaction points that have been identified for these two phytohormones will offer potential genetic intervention strategies to control growth and abiotic stress remediation in future crop breeding programs.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We thank Dr. Pratibha Ravindran for useful discussions. Aach, H. Planta , — Achard, P. Integration of plant responses to environmentally activated phytohormonal signals. Science , 91— The cold-inducible CBF1 factor—dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism.

Plant Cell 20, — Gibberellin signaling controls cell proliferation rate in Arabidopsis. Asano, T. Functional characterisation of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice.

Plant Mol. Bao, G. Plant Biotechnol. Benson, J. Comparison of ent-kaurene synthase A and B activities in cell-free extracts from young tomato fruits of wild-type and gib-1, gib-2, and gib-3 tomato plants. Plant Growth Regul. CrossRef Full Text. Bentsink, L. Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis.

Bi, C. Overexpression of the transcription factor NF-YC9 confers abscisic acid hypersensitivity in Arabidopsis. Burla, B. The expression of Arabidopsis ABA metabolism and signaling genes is regulated through environmental factors. On the other hand, the blue light has a negative impact on the germination of dormant grains in cereals. It indicates that ABA biosynthesis and catabolism take part in blue light—dependent regulation of seed dormancy [ 62 , 63 ].

The high temperature promotes the expression of ABA biosynthesis genes in imbibed seeds, whereas NO positively regulates ABA signaling during seed dormancy breaking [ 52 , 64 ]. PRT6 is E3 ligase promoting protein degradation via 26S proteasome.

The ABA metabolism and signaling genes are also regulated at epigenetic level during the establishment of seed dormancy. GA promotes seed dormancy release and radical protrusion during seed germination. GA biosynthesis takes place mainly in the radicle of the embryo, which in turn ensures germination progression [ 69 ]. Arabidopsis seed germination is associated with the regulation of GA metabolism genes.

Interestingly, ga1 capacity to germinate was renewed after removing testa and endosperm, without exogenous GA application.

The environmental factors, such as light and temperature, interact with GA biosynthesis and signaling, which in turn promotes seed germination.

The expression of GA3ox1 is activated by red light and cold. Additionally, the low temperature determines the GA3ox1 expression localization in the embryonic axis and the aleurone layer [ 71 , 72 ]. Contrarily, low temperature represses the expression of GA catabolism gene, GA2ox2 [ 71 ].

SPT represses germination before stratification, whereas PIL5 also acts as an inhibitor of germination, but after cold stratification in darkness. Furthermore, DAG1 protein binds directly to GA3ox1 promoter, inhibits its expression, and blocks germination [ 74 ]. GA3ox2 activation is associated with summer, whereas GA2ox2 is expressed in winter [ 10 ].

In barley and wheat, the expression of GA biosynthesis genes occurs during imbibition of nondormant seeds [ 31 , 72 ]. Similar reaction was observed during seed dormancy imposed by blue light.

GA metabolism genes are involved in seed dormancy regulation in other monocot species. The regulation of expression of GA synthesis and catabolism genes is more complex in rice.

It resulted in appropriate dormancy phenotype of analyzed cultivars [ 24 ]. Similar analysis was conducted in terms of immature grains of sorghum inbred lines with contrasting dormancy level. To summarize, a proper regulation of GA biosynthesis and catabolism genes ensures the regulation of seed dormancy dependent on environmental conditions, both in dicot and monocot plants.

Overexpression of GID1 promotes the release of seed dormancy. Thus, both mechanisms of seed dormancy loss seem to be regulated differently [ 77 ]. It indicates that SLY1 is the crucial regulator of seed germination [ 79 ]. Another mutant related to GA signaling, cts comatose , maintains seed dormancy even after stratification or after ripening. CTS functions as a peroxisomal ABC transporter and seems to be crucial for seed dormancy release [ 80 ].

Thermoinhibition of seed germination demands activity of RGL2, which suggests its crucial role in the regulation of GA signaling in seeds [ 64 ]. RGL2 activity associates with the regulation of shallow dormancy.

Its expression is promoted during summer time [ 10 ]. The spy mutant demands the lower amount of GA to break seed dormancy and continue germination. Delay of germination 1 DOG1 is considered as the crucial, positive regulator of seed dormancy with unknown function. Expression of DOG1 is seed specific, and dog1 mutant shows disturbed seed dormancy in Arabidopsis [ 83 ]. DOG1 expression is related to deep dormancy during winter season [ 10 ]. Therefore, DOG1 regulates the appropriate time of germination according to environment temperature [ 84 ].

The seed dormancy maintenance or release and further promotion of the seed germination process are regulated by ABA and GA balance [ 1 , 2 , 12 ]. Many molecular interactions between ABA and GA pathways enable precise regulation of seed response according to environmental conditions. The application of paclobutrazol, GA biosynthesis inhibitor, causes better germination of nced9 than the wild type.

ABI4 exerts action on GA biosynthesis genes. The abi4 seeds also accumulate more GA [ 41 ]. The interaction between ABI transcription factors and GA catabolism genes was described in monocot plants. However, the role of MFT is not completely clear. The increased expression of TaMFT is related to the lower germination index, and TaMFT overexpression causes inhibition of precocious germination of isolated embryos.

Low temperature during seed development is associated with a higher level of dormancy. Under such environmental conditions, the activation of TaMFT was observed during seed development [ 92 ].

Probably, the precise role of MFT in seed dormancy is different in dicots and monocots. ABA and GA are not the only phytohormonal regulators of seed dormancy establishment and release. Their action is modulated by other phytohormones, such as auxin, jasmonates JA , brassinosteroids BR , and ethylene.

Auxin promotes seed dormancy release and germination. The role of auxin in the control of seed dormancy includes the action of ABI3. It was observed in parallel with the higher IAA level in seeds during imbibition. Probably, seed dormancy release may be associated with the increased auxin content in seeds of monocot plants.

Regulators of auxin, jasmonic acid, brassinosteroid, and ethylene pathways in seed dormancy promotion or release. The role of JA Jasmonic Acid in seed dormancy is ambiguous. All in all, root growth regulation could be summarized as follows: auxin flows from the lateral root cap to the basal meristem and returns to the root tip Overvoorde et al.

Nitrate is reduced to nitrite by nitrate reductase in the root. Therefore, characterization of ABI5 post-translational modifications is relevant, and it bound to NO interference on acropetal auxin transport through PIN1 auxin efflux carrier, establishes a limited root development Figure 2A. Under low nitrate conditions, because of reduced NO levels, the auxin that is generated in the root contributes to maintain the gradients and maxima required for enhanced root development Ljung et al.

Additionally, in N-starved seedlings, auxin and cytokinins CKs could increase NO production to basal levels, similar to other stresses such as iron deficiency Chen et al. CKs are known to induce NO biosynthesis depending on plant cell status Yu et al. These minimum NO levels would not be enough to repress PIN1 expression, not altering acropetal auxin transport, therefore promoting enhanced root growth Figure 2B. Moreover, ABI5 post-translational state could regulate their downstream transcription factors in an exquisite way, causing an effect in metabolism, growth and plant development.

In Arabidopsis seeds, dormancy release can be activated by cold, nitrate and light. The efficiency of this activation depends on the extension of the dry after-ripening period following harvest Finch-Savage et al.

Light is essential for germination, though dormancy is not released by light if seeds have not been subject to an extended period of after-ripening or a combination of a shorter period of after-ripening plus imbibition on a nitrate solution or cold treatment.

Regulation of seed germination under an excess of nutrient supply has also been deeply studied. CHO1 codes for a putative transcription factor with two AP2 domains, expressed predominantly in seed, with the strongest expression 24 h after seed imbibition.

As a result, both abi4 and cho1 mutants exhibit growth resistance to high concentrations of glucose. The inhibitory action of different sugars on seed germination could proceed through different pathways, including complex interactions with those on phytohormone-response. This suggests that at least some aspects of sugar signaling may be mediated by ABA response Arroyo Becerra et al.

Several sugars may delay seed germination via different pathways. Price et al. Seed germination of Lotus japonicus was reported to be delayed by exogenous glucose Zhao et al.

Inhibition of seed germination by glucose was substantially alleviated by exogenous supply of SNP sodium nitroprusside , an exogenous donor of NO, 2.

At these concentrations, nitrite and nitrate alleviated glucose-induced delay of seed germination. Auxins have been involved in cell-wall remodeling Swarup et al.

In short, seed germination is controlled by nutrient status through multiple action points. This implies a bona fide perception of nutrient balance, acting through signaling pathways either repressing or promoting seed germination. C-status ultimately controls many aspects of plant development. Vegetative growth is controlled by the cellular metabolic status Lastdrager et al.

Sugars are long-distance signals and there are sugar-dependent regulatory networks in roots. Sugar-phosphates regulate plant SnRK1 Ghillebert et al. Sucrose promotes the accumulation of T6P by inhibiting SnRK1 activity, thereby inducing biosynthetic processes and plant growth.

Plant SnRK1 controls several important enzymes, such as nitrate reductase and sucrose phosphate synthase Purcell et al. All these bZIP factors are expressed specifically in sink organs like young leaves, anthers and seeds.

Two Arabidopsis protein kinases, KIN10 and KIN11, seem to be involved in the control of transcription convergent reprogramming as a response to darkness, sugar and stress conditions, three apparently unrelated factors; in addition, specific bZIP transcription factors partially mediate primary KIN10 signaling. Hexokinases play an important role in a hexokinase-dependent sugar response pathway Moore et al. The hexokinase-signaling pathway might play a role in cell-cycle control linked to the carbohydrate status, and sugar regulation of cycD2 seems to be mediated by hexokinase Riou-Khamlichi et al.

Arabidopsis HXK1 plays a relevant role in a number of glucose responses, namely cell proliferation, root and inflorescence growth, leaf expansion and senescence, and reproduction.

HXK1 can play different functions in glucose signaling and metabolism; in fact, many of these new HXK1 functions can be performed at least partially by catalytically inactive HXK1 mutants Moore et al. Growth promotion or inhibition by HXK1 would depend on glucose concentration, cell type, developmental state, and environmental condition Moore et al. In the absence of nitrate, low glucose level signaling is HXK1 mediated but is independent of ABA and ethylene signaling.

Auxins and CKs present links to sucrose sensing and signaling, and can function as short- and long-distance signaling molecules. They can play a role in integration of growth and development between shoot and root Ljung et al. Auxin biosynthesis is induced by soluble sugars, and daily fluctuations in sugar content are correlated with fluctuations in auxin levels Sairanen et al.

Auxins and sugars can be transported from shoot to root, inducing lateral root development in order to increase water and nutrients uptake from the soil, in turn increasing shoot growth capacity Ljung et al. Sugars like trehalose 6-phosphate Tre6P is both a signal of sucrose status and a negative feedback regulator of sucrose levels Yadav et al.

Tre6P can affect developmental processes such as shoot branching. The impact of sugar during the systemic regulation of bud outgrowth in response to either decapitation or light intensity has been analyzed by Barbier et al. Axillary buds outgrowth is driven by sugar availability independently of auxin levels. The combination of high sugar levels in shoot and high sugar sink strength in buds high photosynthesis rate drives to high branching.

Sugars play a signaling role, and not only a trophic role Barbier et al. Figure 3. Molecular components of sugar signaling networks and their involvement in shoot growth. CKs, auxins and sugars function as long-distance signals. When photosynthesis takes place, sugars content increase in shoot and low sugars in roots implies that GAs are transported from the roots to the shoots and send sugars to the low sugar roots. Sucrose availability high metabolic status shows a good correlation with the level of plant T6P, which acts as an inhibitor of SnRK1.

Slower growth at night in the starchless mutant, which shows higher sucrose levels during the day and absence of sugars at the end of the night Wiese et al. The dwarfism of GA-deficient mutants is, instead, uncoupled from carbon availability Ribeiro et al. Cell expansion in the elongation zone of growing roots is controlled by GA, and the endodermis plays a key role in this process.

The Phytochrome-Interacting Factor PIF family of transcription factors seem to have their basic helix-loophelix in every process involving light, temperature and growth De Lucas and Prat, PIFs attenuate the light signal through negative feedback on phytochrome transcription, as well as by bringing them along when they are targeted for proteasome-mediated degradation Ni et al. A combination of circadian clock and light regulation control the activity of PIF4 and PIF5, leading to predictable daily oscillations in seedling growth rates Nozue et al.

These PIF-driven growth cycles depend on supplying seedlings with exogenous sucrose Liu et al. We must consider the matrix effect, since phosphorylation and binding of distinct subsets of these enzymes seem to be regulated by photosynthesis and hormones Coruzzi and Zhou, When cells are starved of metabolizable sugars, binding is lost and its targets are clipped by a specific cysteine protease.

Further studies are required to elucidate the signals responsible for nutrient signaling pathways in the regulation of root and shoot growth.

CKs, auxins, GAs and sugars function as long-distance signals and a low level of sugar in roots implies that GAs are transported from the roots to the shoots. It is known that metabolic events associated with a high concentration of carbohydrates could be crucial rather than the high concentrations of carbohydrate Krapp et al.

In their absence, an additional loss of function of NRT2. However, additional studies are required in order to elucidate how NRT2. KEG plays a relevant role in promoting post-germinative growth Stone et al. The ATL31 protein localizes to the membrane and recruits target proteins for ubiquitination and degradation by the 26S proteasome, allowing seedling development proceed through the early post-germinative growth arrest checkpoint Sato et al.

Protein kinases catalyze ATL31 phosphorylation, which binds to proteins and mediates their stability. Studies carried out by Peng et al.

SnRK1s proteins are known to phosphorylate several targeting proteins, which play a role in C and N metabolism, such as nitrate reductase NR and sucrose 6-phosphate synthase SPS; Comparot et al. Genome-wide analysis due to C and N signaling interactions in Arabidopsis revealed that C is a more ubiquitous regulator of the genome than N Palenchar et al.

Two transcriptional mechanisms are suggested: i independent regulation of C-element and C-Nelement and ii dependent regulation of N-dependent enhancer of C regulation on a C-responsive transcription factor and cis element Palenchar et al. Taken together, a complex picture emerges in which nitrate transporters, glutamate receptors, methyltransferases and ubiquitin ligases are acting on multiple levels to integrate C and N signaling interaction pathways and regulate energy and metabolic genes as well as protein expression.

In this review, we have focused on how changes in C and N levels regulate the production of NO, which acts in plant developmental processes through the interaction with phytohormones and other plant growth regulators, using similar molecular elements.

Recent investigations have the goal to shed light on the molecular mechanisms underlying the crosstalk of nutrients with NO and ABA response. It is important to underline that our current understanding of C and N-dependent signaling pathways in seeds germination and plant development is mainly related to the model plant Arabidopsis.

Therefore, it is necessary to elucidate nutrientsensing and signaling pathways in other plants. As a useful application of the knowledge of these molecular mechanisms, development of perennial versions of important grain crops is crucial for the increasing worldwide food demand.

Root branching order is the main determinant of root trait variation among species Picon-Cochard et al. Perennial crops generally have advantages over annuals in maintaining important ecosystem functions, particularly on marginal landscapes or where resources are limited Tilman et al. Therefore, identification and molecular characterization of genes involved in nutrients crosstalk with root development signaling pathways could be the basis for the generation of perennial crops through crop breeding.

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