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Environmental and Experimental Botany 99 (2014) 110– 121

Contents lists available at ScienceDirect

Environmental and Experimental Botany

journa l h om epa ge : www.elsev ier .com/ locate /envexpbot

eview

lant hormones and seed germination

ohammad Miransari a,b,∗, D.L. Smithc

Mehrabad Rudehen, Imam Ali Boulevard, Mahtab Alley, #55, Postal Number: 3978147395, Tehran, IranAbtinBerkeh Limited Co., Imam Boulevard, Shariati Boulevard, #107, Postal Number: 3973173831, Rudehen, Tehran, IranPlant Science Department, McGill University, 21111 Lakeshore Road, Ste. Anne de Bellevue, Quebec, Canada H9X 3V9

r t i c l e i n f o

rticle history:eceived 5 July 2013eceived in revised form 1 November 2013ccepted 6 November 2013

eywords:lant hormonesroteomic analysiseed germinationoil bacteria

a b s t r a c t

Seed germination is controlled by a number of mechanisms and is necessary for the growth and develop-ment of the embryo, resulting in the eventual production of a new plant. Under unfavorable conditionsseeds may become dormant (secondary dormancy) to maintain their germination ability. However, whenthe conditions are favorable seeds can germinate. There are a number of factors controlling seed germi-nation and dormancy, including plant hormones, which are produced by both plant and soil bacteria.Interactions between plant hormones and plant genes affect seed germination. While the activity ofplant hormones is controlled by the expression of genes at different levels, there are plant genes that areactivated in the presence of specific plant hormones. Hence, adjusting gene expression may be an effec-tive way to enhance seed germination. The hormonal signaling of IAA and gibberellins has been presentedas examples during plant growth and development including seed germination. Some interesting resultsrelated to the effects of seed gene distribution on regulating seed activities have also been presented. The

role of soil bacteria is also of significance in the production of plant hormones during seed germination, aswell as during the establishment of the seedling, by affecting the plant rhizosphere. Most recent findingsregarding seed germination and dormancy are reviewed. The significance of plant hormones includingabscisic acid, ethylene, gibberellins, auxin, cytokinins and brassinosteroids, with reference to proteomicand molecular biology studies on germination, is also discussed. This review article contains almost acomplete set of details, which may affect seed biology during dormancy and growth.

© 2013 Elsevier B.V. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1112. Seed germination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1123. Seed dormancy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1124. ABA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1135. Ethylene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1136. Gibberellins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1147. IAA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1158. Cytokinins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1169. Brassinosteroids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11710. Soil microorganisms and production of plant hormones . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117

11. Conclusions and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author at: Mehrabad Rudehen, Imam Ali Boulevard, Mahtab Alley, #55obile: +98 9199219047.

E-mail address: Miransari1@gmail.com (M. Miransari).

098-8472/$ – see front matter © 2013 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.envexpbot.2013.11.005

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, Postal Number: 3978147395, Tehran, Iran. Tel.: +98 2176506628;

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. Introduction

Among the most important functions of plant hormones isontrolling and coordinating cell division, growth and differen-iation (Hooley, 1994). Plant hormones can affect different plantctivities including seed dormancy and germination (Graebert al., 2012). Plant hormones including abscisic acid (ABA), ethyl-ne, gibberellins, auxin (IAA), cytokinins, and brassinosteroids areiochemical substances controlling many physiological and bio-hemical processes in the plant. These interesting products areroduced by plants and also by soil microbes (Finkelstein, 2004;

imenez, 2005; Santner et al., 2009). There are hormone recep-ors with high affinity in the plant, responding to the hormones.ukaryotes and prokaryotes can utilize similar molecules, whichct as hormone receptors (Urao et al., 2000; Hwang and Sheen,001; Mount and Chang, 2002; Santner et al., 2009).

Before a seed can germinate a set of stages must be completed,ncluding the availability of food stores in the seed. Such food storesnclude starch, protein, lipid and nutrients, which become avail-ble to the seed embryo through the activity of specific enzymesnd pathways (Miransari and Smith, 2009). For example, there is

group of proteins called cyctatins or phytocyctatins, which areble to inhibit the activity of cycteine proteinases as inhibitorsf protein degradation and regulators during seed germinationCorre-Menguy et al., 2002; Martinez et al., 2005).

The whole-genome analyses have indicated the set of genes,hich are related to development, hormonal activity and environ-ental conditions in Arabidopsis. Interestingly, Bassel et al. (2011)

ndicated the distribution of genes in different regions of a seedelated to the following processes: (1) dormancy and germination,2) ripening, (3) ABA activities, (4) gibberellins activities, and (5)tresses such as drought.

For example, in region one, seed activity is up or down reg-lated by different genes such as the main dormancy QTL DOG1nd genes, which positively (GID1A and GID1C) or adversely (ABI3,BI1, ABI5) affect germination. The seed dormancy or germination

s determined by the interactive effects between different signals,uch as the germination signals, which promote seed germina-ion by inhibiting the activity of signals, which may result in seedormancy. The network model presented by Bassel et al. (2011)

ndicates the interactions, which may result in transition from seedormancy to germination.

Fu et al. (2005) determined the total number of proteins1100–1300) in the dry and stratified seeds of Arabidopsis or youngeedlings with respect to the time of sampling using gel elec-rophoresis. The properties of 437 polypeptides were indicatedith the use of mass spectrometric method. Accordingly, the pres-

nce of 293 polypeptides was indicated during all stages, 95 atadicle emergence and 18 at the later stages. They also found that26 of polypeptides may be used by different signaling pathways.ne fourth of proteins were utilized for the metabolism of carbo-ydrate, energy and amino acids, and 3% for the metabolism ofitamins and cofactors. The production of enzymes required for theenetic processes increased quickly at the beginning of germinationnd was the highest at 30 h after germination.

Li et al. (2007) investigated also the trend of protein alterationuring different stages of seed germination in four Arabidopsis 12SSPs. Such kind of analyses can be important for the investigationf feeding embryos by the available proteins during germina-ion. Using the two combined methods of 2-DE scheme and masspectrometry the degradation and accumulation of 12S SSPs werevaluated. According to their analyses, 12 SSPs started to accumu-

ate when the process of cell elongation completed in siliques andn seeds during their development.

According to Liu et al. (2013) the following hormonal andignaling processes are likely when a dormant seed (after-ripened)

xperimental Botany 99 (2014) 110– 121 111

germinates. (1) The sensitivity of seed to ABA and IAA decreases.The related genes, which are affected, include SNF1-RELATEDPROTEIN KINASE2, PROTEIN PHOSPHATASE 2C, LIPID PHOSPHATEPHOSPHTASE2, ABA INSENSITIVES, and Auxin Response Factor of UBIQ-UITIN1 genes. (2) Liu et al. (2013). The inhibiting effects of ABA onseed germination are by adversely affecting the genes of chromatinassembly and modification of cell wall and positively affecting theactivity of genes regulating gibberellins catabolic.

(1) The decay of seed germination is also related to the IAAand jasmonates contents of seed. The following genes are ableto regulate the jasmonate levels in seed: 3-KETOACYL COENZYMEA THIOLASE, ALLENE OXIDE SYNTHASE, 12-OXOPHYTODIENOATEREDUCTASE and LIPOXYGENASE. (2) The changes in the expressionof GA 20-Oxidase and GA 3-Oxidase genes also indicate the likelyrole of gibberellins in the germination of dormant after-ripeningseeds (Liu et al., 2013).

It has been indicated that the activity of the enzyme pectinmethylesterases can affect seed germination. The homogalactur-onans of the cell wall are methylestrified by the enzyme affectingthe cell wall porosity and elasticity and hence cell growth and wateruptake. During the process of seed germination the cell wall of theradicle and of the tissues around it must expand. Accordingly, usinga wild and a transgenic type it was indicated that the enzyme cancontribute to the germination of seed by affecting the properties ofthe cell wall (Müller et al., 2013).

The production and activity of plant hormones is controlledby the expression level of relevant genes. Accordingly, differencesin the germination of different seed cultivars are related to theirgene complement. The other important factor that can determinethe expression level of genes in specific plant tissues is their copynumber and hence their necessary concentration required for theirexpression. These kinds of details can be used for the determina-tion of genes functioning at different plant growth stages, as wellas under stress (Miransari, 2012; Miransari et al., 2013a).

Using microarray analyses Ransom-Hodgkins (2009) recognizedfour genes related to the eukaryotic elongation factor (eEF1A) fam-ily, which are expressed during the germination of Arabidopsisthaliana seeds. These genes are also expressed in the embryos andthe meristems of plant shoots and roots. Inhibiting the expressionof any one of the four genes resulted in the formation of seedlingswith stunted roots and the alteration of expression in the otherthree genes.

The protein eEF1A is a multifunctional protein necessary for thefollowing: (1) protein translation, (2) binding actin as well as micro-tubules, (3) bundling actin, and (4) interacting with ubiquitin atthe time of protein degradation (Ransom-Hodgkins, 2009). Thereare other functions performed by eEF1A, including a role in thepathway of various signals, such as phosphatidylinositol 4-kinase(Yang and Boss, 1994), and its role as a substrate for different kinaseenzymes (Izawa et al., 2000). This protein can also regulate theactivities of the DNA replication/repair protein network (Toueilleet al., 2007) and play a role in apoptosis (Ejiri, 2002). There is a setof 2–15 plant genes producing eEF1A proteins (Aguilar et al., 1991).

There are some photoreceptors that are necessary for plantgrowth and development, including seed germination. For exam-ple, phytochrome B proteins, which are stable and found in greentissues (Quail, 1997) are able to regulate the hormonal signalingpathways of auxin and cytokinin (Tian et al., 2002; Fankhauser,2002; Choi et al., 2005). Phytochromes in the seeds are necessaryfor controlling seed germination, especially when the seeds are sub-jected to light. Light activates phytochromes, as well as hormonalactivities in plants (Seo et al., 2009).

Different methods have been used for the extraction ofbio-chemicals, including plant and bacterial products affectingmorphological and physiological processes related to seed develop-ment. Such discoveries in combination with the use of exogenously

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pplied plant hormones (Lian et al., 2000) have led to more rapiddvancement of the field and some interesting findings (Miransarind Smith 2009). Plant hormones are interactive and hence theroduction of each may be dependent on the production of otherormones (Brady et al., 2003; Arteca and Arteca, 2008).

There are different parameters affecting the activities of plantormones including the receptor properties and its affinity for theormone, and cytosolic Ca2+, which, for example, can influencetomatal activities through affecting the K+ channel (Weyers andaterson, 2001). Among their other functions, the effects of plantormones on seed germination may be one of their most important

unctions in plant growth. Hence, in the following such effects areiscussed with respect to proteomic and molecular biology studies,ith a view toward prospects for future research.

. Seed germination

Seed germination is a mechanism, in which morphological andhysiological alterations result in activation of the embryo. Beforeermination, seed absorbs water, resulting in the expansion andlongation of seed embryo. When the radicle has grown out of theovering seed layers, the process of seed germination is completedHermann et al., 2007). Many researchers have evaluated the pro-esses involved in seed germination, and how they are affected bylant hormones in a range of plant families, such as the BrassicaceaeMuller et al., 2006; Hermann et al., 2007).

Seeds contain protein storages, such as globulins and prolamins,hose amounts are increased during seed maturation, especially

t the mid- and late-stages of seed maturation, when seeds absorbarger amounts of nitrogen. These proteins are located in the cell

embrane or other parts of the seed. During the time of proteinranslocation into different parts of the seed, negligible amounts ofrotein are turned into other products. The activation of enzymesuch as proteinase results in the mobilization of storage proteinsWilson, 1986).

Storage proteins are also found in the seedling radicle and shootTiedemann et al., 2000). The mobilization of storage proteins doesot take place at the same time in different parts of the seed. Thether enzymes, which are activated during the mobilization of pro-eins, are carboxypeptidase and aminopeptidase. Among the mostmportant parameters controlling the process of seed dormancyre changes at molecular levels, including the protein and hor-onal alterations, and the balance between ABA and gibberellins

Ali-Rachedi et al., 2004; Finch-Savage and Leubner-Metzger 2006;inkelstein et al., 2008; Graeber et al., 2010). Parameters such as theelated genes, chromatin related factors, and the processes, whichre non-enzymatic, affect seed dormancy. The genes, which controlormancy, include the maturating genes, hormonal and epigeneticegulating genes, and the genes, which control release from dor-ancy (Graeber et al., 2012).Use of mutants is one of the most interesting ways to deter-

ine the role of each plant hormone, in seed germination. Theynthesis of DNA and mitotic microtubules are among the vari-us changes taking place during embryogenesis, and these can besed as the indicators of cell division and differentiation duringhis stage. These processes are paralleled by seed abilities to toler-te desiccation and become dormant (Finkelstein, 2004; de Castrond Hilhorst, 2006).

Seed development includes the formation of the embryo bodyy cell division and differentiation, resulting in the formation ofmbryonic organs (Goldberg et al., 1994; Meinke, 1995). This period

overs the maturation of seed, including the formation of organsnd nutrient storage, as well as changes in the embryo size andeight, followed by the acquisition of desiccation tolerance andormancy (Finkelstein, 2004; de Castro and Hilhorst, 2006). Seed

xperimental Botany 99 (2014) 110– 121

maturation results in inhibition of the cell cycle, decreased seedmoisture, increased ABA levels, production of storage reservoirsand established dormancy (Matilla and Matilla-Vazquez, 2008).

In addition to the effects of plant hormones on seed germinationresearchers have found that both under stress and non-stress con-ditions, N compounds, including nitrous oxide can enhance seedgermination through enhancing amylase activities (Zhang et al.,2005; Hu et al., 2007; Zheng et al., 2009). Through decreasingthe production of O2 and H2O2 such products can also alleviatethe stress by controlling the likely oxidative damage, similar tothe effects of antioxidant enzymes including superoxide dismutase(SOD), catalse (CAT) and peroxidase (POD) on plant growth undervarious stresses (Song et al., 2006; Tian and Lei, 2006; Tseng et al.,2007; Li et al., 2008; Tuna et al., 2008; Zheng et al., 2009; Sajediet al., 2011).

In addition, N products can enhance seed germination byadjusting K+/Na+ ratio and increasing ATP production and seed res-piration (Zheng et al., 2009). The allelopathic effects of seeds canalso positively or adversely affect the germination of their own orother plant seeds (Ghahari and Miransari, 2009). Proteomic analy-sis of seed germination in Arabidopsis thaliana indicated that duringthe process of seed germination 74 proteins are altered before radi-cle emergence and protrusion (Gallardo et al., 2001).

Using proteomic analysis it is possible to identify proteins, theirfunctions and interactions as well as their subcellular localizationin a tissue or an organelle. This can be useful for the determina-tion of protein alteration during plant development, including theformation of specific tissues and organelles, as well as seed ger-mination. Accordingly, use of proteomics has become increasinglycommon in cellular, genetic and physiological research (Pandy andMann, 2000). For example, the proteomic analysis of rice (Orizasativa cv Nipponbare) tissues including leaf, root and seed usingelectrophoresis, mass spectrometry and multidimensional proteintechnology indicated the presence of 2528 unique proteins (Kolleret al., 2002).

3. Seed dormancy

Seed dormancy is a mechanism by which seeds can inhibittheir germination in order to wait for more favorable conditions(secondary dormancy) (Finkelstein et al., 2008). However, primarydormancy is caused by the effects of abscisic acid during seed devel-opment. Such seeds may never germinate (Bewley, 1997). Usuallyfreshly harvested seeds of plants like barley (Hordeum vulgare L.) arenot able to germinate at temperatures higher than 20 ◦C (Corbineauand Come, 1996; Leymarie et al., 2007). In barley the process ofdormancy is due to the fixation of oxygen by glumellae during theoxidation of phenolic products, resulting in the limitation of oxygensupplement to the embryo. The resulting hypoxia may also inter-fere with ABA activities in the seed (Benech-Arnold et al., 2006).

Gibberellins are able to activate dormant seeds, although thehormone does not control seed dormancy (Bewley, 1997; Miransariand Smith, 2009). ABA can inhibit corn germination by affecting thecell cycle. This is the reason for the more rapid germination of seedsthat are deficient in ABA. Inhibition of the cell cycle by ABA is relatedto activation of a residual G1 kinase, which becomes inactivated inthe absence of ABA (Sanchez et al., 2005).

By affecting hormonal balance in the seed, environmentalparameters including salinity, acidity, temperature and light, caninfluence seed germination (Ali-Rachedi et al., 2004; Alboresi et al.,2006). Nitrate (NO3

−) and gibberellins are able to enhance seed

germination. NO3

− can act as a source of N and a seed germina-tion enhancer. Similarly, gibberellins enhance seed germination byinhibiting ABA activity. It is caused by the activation of catabolyzingenzymes and inhibition of the related biosynthesis pathways,

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hich also decreases ABA amounts (Toyomasu et al., 1994; Atiat al., 2009). Enzymes including nitrite reductase, nitrate reduc-ase, and glutamine synthetase assimilate NO3

− into amino acidsnd proteins.

Salinity decreases seed germination by affecting the seed nitro-en (N) content and hence embryo growth. This indicates how Nompounds can alleviate the stress of salinity on seed germinationAtia et al., 2009). N can also inhibit seed dormancy by decreasinghe level of ABA in the seed (Ali-Rachedi et al., 2004; Finkelsteint al., 2008). The unfavorable effects of salinity on seed germina-ion include: (1) decreasing the amounts of seed enhancer productsncluding NO3

− and gibberellins, (2) enhancing ABA amounts, and3) altering membrane permeability and water behavior in the seedKhan and Ungar, 2002; Lee and Luan, 2012).

ABA and gibberellins are necessary for dormancy initiation andeed germination, respectively (Groot and Karssen, 1992; Matilland Matilla-Vazquez, 2008). The gibberellins/ABA balance deter-ines seed ability to germinate or the pathways necessary for seedaturation (White et al., 2000; White and Rivin, 2000; Chibani

t al., 2006; Finch-Savage and Leubner-Metzger, 2006). WhileBA determines seed dormancy and inhibits seed from germina-

ion, gibberellins are necessary for seed germination (Matilla andatilla-Vazquez, 2008).Although seed dormancy is under the influence of plant hor-

ones, seed morphological and structural characteristics such asndosperm, pericarp and seed coat properties can also affect seedormancy (Kucera et al., 2005). Both ethylene and gibberellinsffect radicle growth, with gibberellins being the most importantormone. Although gibberellins are necessary for the productionf mannanase, which is necessary for seed germination, ethyl-ne is not (Wang et al., 2005a,b). However, in gibberellin deficientutants, ethylene can act similar to gibberellins, because the seeds

re able to germinate completely in such a situation (Karssen et al.,989; Matilla and Matilla-Vazquez 2008).

Using proteomic analyses the molecular and biological stageselated to seed germination have been elucidated. At differenttages of seed germination, expression of different genes resultsn the production of proteins, necessary for seed germination andormancy release. Proteins necessary for seed germination areccumulated after-ripening, under seed drying conditions, result-ng in the release of dormancy (Gallardo et al., 2001; Chibani et al.,006).

. ABA

While ABA positively affects stomatal activity, seed dormancynd plant activities under stresses such as flooding (abiotic) andathogen presence (biotic) (Moore, 1989; Davies and Jones, 1991;eyers and Paterson 2001; Popko et al., 2010), it adversely affects

he process of seed germination. For example, concentrations of–10 �M can inhibit seed germination in plants like Arabidopsishaliana (Kucera et al., 2005; Muller et al., 2006). However, otherlant hormones including gibberellins, ethylene, cytokinins, andrassinosteroids, as well as their negative interaction with ABA, canositively regulate the process of seed germination (Kucera et al.,005; Hermann et al., 2007). Under stress ABA can be quickly pro-uced as a �-glucosidase (Lee et al., 2006). Additionally, it has been

ndicated that phosphatase regulators can also act as ABA receptorsMa et al., 2009).

The movement of ABA across the cellular membrane is underhe influence of pH and cellular compartment. Hence, it is likely

o predict the hormone concentration in different cellular com-artments, according to its cellular pH and compartment. Differentxperiments have demonstrated that the receptors for ABA and IAAre located outside the plasma membrane (Weyers and Paterson,

xperimental Botany 99 (2014) 110– 121 113

2001), indicating that sometimes the appoplasm may be the impor-tant compartment. Soluble factors, F-box proteins, are receptors forIAA (Dharmasiri et al., 2005a,b; Kepinski and Leyser, 2005; Santneret al., 2009). For ABA, one family of proteins called PYR/PYL/PARis the receptor (Park et al., 2009). IAA is the most important hor-mone for the process of somatic embryogenesis (Cooke et al., 1993;Jimenez, 2005). Researchers have recently found two new G pro-teins, which are ABA receptors (Pandey et al., 2009).

The role of ABA and its responsive genes in the process ofseed germination has been indicated (Nakashima et al., 2006;Graeber et al., 2010). The inhibitory effects of ABA on seed ger-mination is through delaying the radicle expansion and weakeningof endosperm, as well as the enhanced expression of transcriptionfactors, which may adversely affect the process of seed germina-tion (Graeber et al., 2010). The gibberrelin repressor RGL2 is able toinhibit seed germination by stimulating the production of ABA aswell as the related transcription factors (Piskurewicz et al., 2008).The H subunit of a chloroplast protein, Mg-chelatase can act as ABAreceptor during different growth stages of plant including seed ger-mination (Shen et al., 2006). It has recently been suggested thatGPROTEIN COUPLED RECEPTOR 2 can also act as another ABA recep-tor, mediating different activities of ABA, including its effects onseed germination (Liu et al., 2007b). However, other researchersindicated that such a receptor is not necessary for activities medi-ated by ABA, including the process of seed germination (Johnstonet al., 2007; Guo et al., 2008).

5. Ethylene

Compared with the other plant hormones, ethylene has the sim-plest biochemical structure. However, it can influence a wide rangeof plant activities (Arteca and Arteca, 2008). Similar to cytokinin,the perception of ethylene is by a kinase receptor, which is a two-component protein. However, for ethylene the receptor is locatedin the membrane of endoplasmic reticulum (Kendrick and Chang,2008; Santner et al., 2009). Although ethylene can affect differ-ent plant activities, including tissue growth and development, andseed germination, however it is not yet understood how ethyleneinfluences seed germination. There are different ideas regardingseed germination; according to some researchers ethylene is pro-duced as a result of seed germination and according to the otherresearchers ethylene is necessary for the process of seed germina-tion (Matilla, 2000; Petruzzelli et al., 2000; Rinaldi, 2000).

Ethylene is able to regulate plant responses, under a rangeof conditions, including stress. For example, in combination withABA, ethylene is able to affect plant response to salinity. Underincreased levels of salinity, ethylene production in plants increases,which decreases plant growth and development. The enzyme 1-aminocyclopropane-1 carboxylic acid (ACC) is a pre-requisite forethylene production, catalyzed by ACC oxidase. During the timethat seed is exposed to the stress, ethylene production is affected(Mayak et al., 2004; Jalili et al., 2009).

The amount of ethylene increases during the germination ofmany plant seeds including wheat, corn, soybean and rice, affectingthe rate of seed germination (Pennazio and Roggero, 1991; Zapataet al., 2004). ACC can enhance seed radicle emergence through theproduction of ethylene, produced in the radicle (Petruzzelli et al.,2000, 2003). With respect to the easy production of ethylene fromACC in the presence of ACC oxidase, ACC has been widely tested innumerous experiments (Petruzzelli et al., 2000; Kucera et al., 2005).

It has been indicated that during the final stage of seed ger-

mination ethylene is produced in different plant species andit can contribute to the germination of seeds after dormancy.Ethylene is produced through the pathway that turns S-adenosyl-Met into 1-Amicocyclopropane-1-carboxillic-acid (ACC) by ACC

114 M. Miransari, D.L. Smith / Environmental and Experimental Botany 99 (2014) 110– 121

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ynthase, followed by the oxidation of ACC to ethylene by ACC oxi-ase (Yang and Hoffman, 1984; Kende, 1993; Argueso et al., 2007).he amounts of ethylene increase under stress and it can controlumerous processes in plants, including flowering, fruit ripening,ging, dormancy inhibition and seed germination (Matilla, 2000;ath et al., 2006; Matilla and Matilla-Vazquez, 2008).

As previously mentioned, ethylene is also important duringtress and its production and hence plant growth is affectedDruege, 2006). Researchers have indicated that ethylene in plantsncreases under stress, which can decrease plant growth, includ-ng that of plant roots. Interestingly, they have also found that theacterial enzyme ACC deaminase is able to alleviate such stressesy degrading the ethylene pre-requisite ACC (Mayak et al., 2004).thylene can also influence plant performance by affecting theroduction and functioning of other hormones, for example byffecting the related pathways (Arora, 2005; Vandendussche andan Der Straeten, 2007).

The membrane localized receptors of Arabidopsis, which areecessary for the perception of ethylene are activated by severalenes including ETR1, ERS1, ETR2, ERS2 and EIN4 with the follow-ng domains: (1) N-terminal for biding ethylene, (2) C-terminaleceiver (not present in the ERS1 and ERS2 genes) and (3) histi-ine protein kinase. As a result of ethylene binding such receptorsecome inactive (Gallie and Young, 2004). However, only two ofuch genes are necessary for the activation of maize localized-embrane receptors as well as for the activation of ACC synthase

nd ACC oxidase, for example in the endosperm and embryo. Theigh expression of ethylene receptors in the embryo can enable thembryo to grow.

Brassinosteroids (BR) and IAA are able to stimulate the produc-ion of ethylene (Arteca and Arteca, 2008). Gibberellins, ethylenend BR can induce seed germination by rupturing testa andndosperm, while antagonistically interacting with the inhibitoryffects of ABA on seed germination (Finch-Savage and Leubner-etzger, 2006; Holdsworth et al., 2008; Finkelstein et al., 2008).

thylene is able to make dormant seeds germinate. It has beenuggested that by regulating the expression of cysteine-proteinaseenes, and its protein complex, proteasome, ethylene can removeeed dormancy (Asano et al., 1999; Borghetti et al., 2002). These

cognition of DELLA proteins, and hence the lifting of gibberellins DELLA repression. DELLA repression. (C) DELLA phosphorylation adversely affects DELLA responding.

merican Society of Plant Physiologists; American Society of Plant Biologists).

enzymes can degrade seed proteins during the first stages of ger-mination.

The novel mechanism by which ethylene inhibits the adverseeffects of ABA on the release of seed dormancy has been attributedto the production of OH in the apoplasm. Production of reactiveoxygen species in the apoplasm can also affect seed germination(Chen, 2008; Muller et al., 2009; Graeber et al., 2010). Reactiveoxygen species are produced at different stages of seed growthand development. Usually reactive oxygen species adversely affectseed activities. However, some new findings indicate that there arealso some positive effects for reactive oxygen species, includingthe germination of seeds and the growth of seedlings by the reg-ulation of cell growth and development, as well as by controllingpathogens and cell redox conditions. Reactive oxygen species mayalso positively affect the release of seed dormancy by interactingwith gibberellin and abscisic acid transduction pathways, affect-ing many transcriptional factors and proteins (El-Maarouf-Bouteauand Bailly, 2008).

6. Gibberellins

Gibberellins are diterpenoid, regulating plant growth. They arecommonly used in modern agriculture and were first isolated fromthe metabolite products of the rice pathogenic fungus, Gibberellafujikuroi, in 1938 (Yamaguchi 2008; Santner et al., 2009). Thebiosynthesis of gibberellins is from geranyldiphosphate througha pathway including several enzymes. Gibberellins are adverselyregulated by DELLA proteins, with a C-terminal GRAS domain intheir structure, which are eventually degraded by the E3 ubiquitinligase SCF (GID2/SLY1) (Itoh et al., 2003; Schwechheimer 2008).

Accumulation of DELLAs in seeds can result in the expres-sion of genes producing F-box proteins. The gibberellins receptorhas recently been identified in rice. It is GIBBERELLINE INSEN-STIVE DAWRF1 (GID1) protein (interacting with DELLA proteinsand resulting in their eventual degradation) located in the nucleus,

and can bind to the gibberellins, which are biologically active (Fig. 1)(Ueguchi-Tanaka et al., 2005; Griffiths et al., 2006; Nakajima et al.,2006; Willige et al., 2007). Through its antagonistic effects withABA, gibberellins, which are internal signals, are able to release

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eeds from dormancy (Gubler et al., 2008; Seo et al., 2009). In Ara-idopsis thaliana the three receptors, GID1a, GID2b, and GID2c acts gibberellins receptors. The weakening of endosperm is by thectivation of gibberellins genes affecting the modifying proteinsf cell wall (Voegele et al., 2011). However, ABA can prevent theeakening of endosperm (Muller et al., 2006; Linkies et al., 2009).

The seed endosperm, which becomes available to the embryo,hrough the activities of some hydrolase enzymes, is made of thetarchy part of the seed and the surrounding aleurone (Jones andacobsen, 1991; Bosnes et al., 1992). Gibberellins stimulate theynthesis and production of the hydrolases, especially �-amylase,esulting in the germination of seeds. Gibberellins are able to induce

range of genes, which are necessary for the production of amy-ases including �-amylase, proteases and �-glucanases (Applefordnd Lenton, 1997; Yamaguchi, 2008). Different processes in theeed indicate that seed aleurone is appropriate for the evaluationf transduction pathways at the time of plant hormones produc-ion, including gibberellins (Ritchie and Gilroy, 1998; Penfield et al.,005; Achard et al., 2008; Schwechheimer, 2008).

The plant hormone gibberellins are necessary for seed germi-ation. The Signaling pathways of hormone can stimulate seedermination through the release of coat dormancy, “weakening ofndosperm”, and “expansion of embryo cell”. Proteins resultingn the modification of cell wall like xyloglucan endotransglyco-ylase/hydrolases (XTHs) and expansins may enhance the aboveentioned pathways (Liu et al., 2005; Voegele et al., 2011). The

nteresting mechanism, which controls seed germination, is theuppressing effects of excess ABA on embryo expansion, whichnhibit the promoting effects of gibberellins on radicle growth,nd hence it will not germinate through the endosperm and testaNonogaki, 2008).

It has been indicated that there is an intimate interactionetween gibberellins metabolism and gibberellins response path-ays. This kind of interaction, along with other pathways in thelant, results in the regulation of plant growth and development.sing proteomic analysis Gallardo et al. (2002) indicated the wayia which the germination of Arabidopsis seeds is regulated by gib-erellins. In this kind of interaction, the �-tublin a component ofhe cytoskeleton is affected by the hormone.

Expression of the Osem gene is regulated by gibberellins as wells by ABA. This gene is homologous to the Em gene of wheat,hich regulates the production of one of the embryogenesis abun-ant proteins. Gibberellins are able to influence leaf growth byegulating the activity of lactoylglutathione lyase (Hattori et al.,995). Gibberellins upregulation of photosystem II oxygen produc-ion may enhance the efficiency of energy pathways in plant tissues.his may also be the case in germinating seedlings (Finkelstein et al.,002).

Gibberellins are also able to regulate the activity of RPA1 (repli-ation protein A1) gene, which are found in significant amountsn tissues with actively dividing cells (Van der Knaap et al., 2000),s well as the activity of plant receptors, such as kinases. In addi-ion, gibberellins can influence the production of proteins duringathogenic, oxidative and heavy metal stress (Marrs, 1996).

The regulation of proteins, with a range of functions, in cul-ured cells by gibberellins is also of significance. These proteinsnclude the ones regulating metabolism (formate dehydrogenase),ranscription (nucleotide binding proteins), protein folding (chap-ronins), energy (GADPH), signal transduction (G proteins), andell growth (GF14-c protein) (Olszewski et al., 2002). Plant growthnd development is significantly affected by the cross talk betweenlant hormones (Davies, 1995). The activity of plant genes is usu-

lly regulated by more than one plant hormone (Yang et al., 2004;epuydt and Hardtke, 2011).

The activity of genes regulated by gibberellins is adverselyffected by ABA. In their research, constructing a cDNA microarray

xperimental Botany 99 (2014) 110– 121 115

(with about 4000 genes), Yang et al. (2004) identified some rice seedgenes, regulated by gibberellins and brassinosteroids. However,to identify more gibberellins and brassinosteroids related genesuse of cDNA, with more genes as well as use of mutants is nec-essary. This kind of analysis may result in more details regardingthe activity and role of the hormones. The important point, whichmust be indicated about gibberellins, is to indicate if DELLA abilityto bind to GID1 or other proteins can be influenced by modifyingposttranscriptional. DELLA controlling of plant development is byZIM domain control JAZ1 and bHLH and GRAS transcription factors(Hauvermale et al., 2012a,b).

7. IAA

Auxin is a plant hormone, which plays a key role in regulatingthe following functions: cell cycling, growth and development, for-mation of vascular tissues (Davies, 1995) and pollen (Ni et al., 2002),and development of other plant parts (He et al., 2000a). The growthand development of different plant parts, including the embryo,leaf and root is believed to be controlled by auxin transport (Liuet al., 1993; Xu and Ni, 1999; Rashotte et al., 2000; Benjamins andScheres, 2008; Popko et al., 2010). Such kind of regulation is byaffecting the transcriptional factors (Hayashi, 2012).

Auxin is bound to AFB receptors as the subunits of ligase com-plex of SCF ubiquitin. The specificity of auxin regulated genes isdetermined by the following: the related proteins, the regulationof their post transcripts, their related stability and the affinitybetween the related proteins. The protein ABP1 is the auxin bind-ing protein, which can act as a receptor in the non- transcriptionalsignaling of auxin. ABP1 is also able to mediate the genes regulat-ing the activity of AFB receptors. Hence, both ABP1 and AFB are ableto regulate the physiological activities of auxin. Another importantfunction defined for auxin is elongation of cell, which is done non-transcriptionally with the help of ABP1 activating the expressionof AUX/IAAs genes. Such kind of receptors regulates the signalingresponses of auxin during cell cycling. Gibberellins can also simi-larly affect cell cycling in plant (Hauvermale et al., 2012a,b).

Auxin by itself is not a necessary hormone for seed germina-tion. However, according to the analyses regarding the expressionof auxin related genes, auxin is present in the seed radicle tip dur-ing and after seed germination. In addition, microRNA60 inhibitsauxin RESPONSE FACTOR10 during seed germination so that theseed can germinate. Such a controlling process is also neces-sary for the stages related to post-emergence growth, includingseed maturation. The mechanisms for such inhibitory effects havebeen attributed to interactions with the ABA pathway (Liu et al.,2007a, b). Although IAA may not be necessary for seed germina-tion, it is necessary for the growth of young seedlings (Bialek et al.,1992; Hentrich et al., 2013). The accumulated IAA in the seed cotyle-don is the major source of IAA for the seedlings. In legumes, amideproducts are the major source of IAA in mature seeds (Epstein et al.,1986; Bialek and Cohen, 1989).

There are some AUXIN RESPONSE FACTORS acting as tran-scription factors and controlling different stages of plant growthand development. For example, in Arabidopsis thaliana such genesare influenced by microRNA’s, which are small (with 21–24nucleotides) single stranded RNA’s, affecting gene activity at post-transcriptional level (Bartel, 2004). Among the most importanteffects of microRNA’s are the followings: (1) plant growth, (2)hormonal signaling, (3) homeostasis and (4) responses to environ-mental and nutritional alterations (Juarez et al., 2004; Liu et al.,

2007a, b). MicroRNA’s are able to regulate a number of hormonaltransduction pathways.

For example, the activity of gibberellins is regulated bymicroRNA’s in the presence of DELLA proteins. During the

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egulation of auxin activity (its signal transduction pathway) byicroRNA’s, auxin binds its receptor, which is an F-box protein

nd proteolyses the AUX/IAA proteins. These proteins interactith ARFs by binding the auxin response elements and activate

r repress the activity of the related genes (Ulmasov et al., 1997,999).

Researchers have successfully used microRNA-resistantutants to determine how ARFs may function biologically. They

ound that the down regulation of these ARF’s is necessary forhe growth and development of root, leaf and flower. Using seednd seedling of mutants, the important role of auxin signalingathways during the first stages of seedling development wasetermined. The importance of microRNA’s and ARF’s affectinghe interaction of auxin and ABA during the stages of germinationnd post germination was clarified (Liu et al., 2007a, b). Mutationn some of genes, such as ibr5 (indole-3-butyric acid-response), with some similarity to MAPK (mitogen-activated proteininase) phosphatases decreases their sensitivity to auxin as wells the response of roots to ABA, and increases the rate of seedermination in the presence of ABA (Monroe-Augustus et al.,003).

Accordingly, the adverse effects of microRNA160 on ARF10 canffect the processes of seed germination and post germination (Liut al., 2007a, b). In transgenic plants the resistance of ARF10, versusicroRNA activity may result in growth defects of some plant parts

ncluding leaf, flower and stem. The ARF10 mutant plants indicate high level of sensitivity to ABA. Similarly, exogenous IAA can alsoesult in such responses by a wild-type plant. However, it is likelyo decrease seed sensitivity to ABA by overexpressing microRNAsLiu et al., 2007a, b).

The most important plant hormones for seed germination areBA and gibberellines, which have inhibitory and stimulatoryffects on seed germination, respectively. BR and ethylene also havenhancing effects on seed germination. Although IAA by itself mayot be important for seed germination, its interactions and crossalk with gibberellins and ethylene may influence the processesf seed germination and establishment (Fu and Harberd, 2003;hiwocha et al., 2005).

Alteration of the auxin signaling pathway, by altering auxinesponse factor, increases seed sensitivity to ABA, as mRNA60 mayffect the ABA responsive gene by repressing auxin response fac-or (Liu et al., 2007a, b). Auxin can influence seed germination,hen ABA is present (Brady et al., 2003). Accordingly, mRNA60 is

ble to regulate the cross-talk between IAA and ABA. However, theolecular mechanism regulating the interactions and cross-talk

etween IAA and ABA is not known yet. IAA is also able to affecteed germination by affecting the activity of enzymes for example,n germinating pea seeds, the activity of glyoxalase I was regulatedy IAA, resulting in higher rates of cell growth and developmentThornalley, 1990; Hentrich et al., 2013).

. Cytokinins

Cytokinins are derived from adenine molecules in which theres a side chain at the N6 position. Miller was the first to dis-over them, in the 1950s, based on their ability to enhance plantell division (Miller et al., 1955). Cytokinins are plant hormones,egulating a range of plant activities including seed germination.hey are active in all stages of germination (Chiwocha et al., 2005;ikolic et al., 2006; Riefler et al., 2006). They can also affect thectivities of meristemic cells in roots and shoots, as well as leaf

enescence. In addition, they are effective in nodule formation dur-ng establishment of the N2-fixing symbiosis and other interactionsetween plant and microbes (Murray et al., 2007; To and Kieber,008; Santner et al., 2009). The production of active cytokinins is

xperimental Botany 99 (2014) 110– 121

through the activity of a phosphoribohydrolase enzyme, turningthe nucleotide into a free base (Santner et al., 2009).

Signaling in cytokinins is very similar to the two-componentsignaling in the bacterial species (To and Kieber 2008). In thiskind of perception, the initiation of phosphorelay by ligand bind-ing is related to kinases histidine and asparate. The perceivingcompounds, which are in nucleus, are able to phosphorylate theresponse proteins, which can negatively or positively regulatecytokinin signaling. Similar to auxin, cytokinins are also able toregulate many genes, including CYTOKININ RESPONSE FACTORS(Rashotte et al., 2003; Santner et al., 2009).

The cytokinin receptors (Arabidopsis thaliana) are able to regu-late different functions related to the development and physiologyof Arabidopsis thaliana. They include AHK2, AHK3 and CRE1/AHK4with the following activities. (1) Embryo development by affect-ing the cellular division, which subsequently causes the vesicularto differentiate, (2) seed size, (3) seed production and germina-tion, (4) hypocotyls and shoot growth, (5) senescence of leaf, (6)root growth, (7) nutrient uptake, (8) handling stress (Riefler et al.,2006; Heyl et al., 2012). However, in the other plants the functionsof cytokinin receptors (MtCRE1, LjCRE1, LaHK1, MsHK1, and BpCRE1PtCRE1) include: (1) root production and growth, (2) symbiosis pro-cess, (3) formation of root nodules, and (4) nodule senescence (Cobade la Pena et al., 2008a,b; Heyl et al., 2012).

The following indicates the interactions, which may existbetween the cytokinin receptor and the related ligand. (1) Thereis a high affinity between cytokinin receptors and most naturalcytokinins, which are active, (2) the receptors has only one sitefor ligand binding, (3) the affinity of cytokinin receptors to the dif-ferent cytokinins is determined by their activities in the bioassays,(4) cytokinin can firmly bind over a wide range of conditions, (5)the cytokinin receptors of Arabidopsis thaliana and maize indicatesimilar properties (Heyl et al., 2012).

Although there is some finding about cytokinin receptors, thereare yet more to be learnt regarding cytokinin receptors. The detailsregarding the three dimensional structure of the receptor domainand its related evolution may significantly indicate some importantand new details related to the action of cytokinin receptors. Forexample, how the receptors may transfer signal from and acrossthe membrane to the cytoplasm. Considering plant shoot and root,as the action sites of receptors, it must be yet indicated whichactivities of cytokinins are regulated by their receptors (Heyl et al.,2012).

Cytokinins are also able to enhance seed germination by thealleviation of stresses such as salinity, drought, heavy metals andoxidative stress (Khan and Ungar, 1997; Atici et al., 2005; Nikolicet al., 2006; Peleg and Blumwald, 2011). They can be inactivatedby the enzyme cytokinin oxidase/dehydrogenase (Galuszka et al.,2001) catalyzing the cleavage of their unsaturated bond. Differentactivities of cytokinins, such as their effects on seed germination,have been attributed to the various functions of cytokinins in dif-ferent cell types (Werner et al., 2001).

Arabidopsis thaliana has three histidine kinases that can act asreceptors for cytokinins (Inoue et al., 2001; Yamada et al., 2001).Controlling seed size, including embryo, endosperm and seed coatgrowth, is also among the functions of cytokinins. Endosperm andseed coat growth in Arabidopsis is followed by embryo growth, ata later stage of embryogenesis, which is less related to the finalseed size (Mansfield and Bowman, 1993). There are several factorscontrolling seed number with respect to the number of seeds, andthe most important of these is the available carbon source for seedutilization (Riefler et al., 2006).

Subbiah and Reddy (2010) investigated the interactive effectsof different plant hormones on seed germination in an ethylene-related mutated Arabidopsis. The mutation of etr1 and ein2genes, which adversely affects the ethylene response, resulted in

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nhanced seed dormancy and delayed seed germination related tohe wild type. Mutated etr1, ein2 and ein6 also resulted in enhancedesponse to ABA with respect to its inhibitory effects on seedermination. However, mutation of ctr1 and eto3 genes, which sig-ificantly enhance ethylene response and production, decreasedeed sensitivity to ABA at germination. Use of AgNO3 also increasedensitivity to ABA during germination through its inhibitoryffects on ethylene activity. However, addition of cytokinin N-6enzyl adenine (BA) decreased the enhanced response of ethylene-esistant mutants to ABA, indicating that not all effects of cytokininn seed germination are through its effects on ethylene activity.

. Brassinosteroids

Brassinosteroids (BR) are a class of plant hormones, similar tohe steroid hormones in other organisms (Rao et al., 2002; Bhardwajt al., 2006; Arora et al., 2008). The cholestane hydroxylated deriva-ives produce BR and the C-17 side chain and rings and the relatedeplacements determine the variations in the hormonal structureArora et al., 2008). BR has a wide range of activities in plant growthnd development including cell growth, vascular formation, repro-uctive growth, seed germination, and production of flowers andruit (Khripach et al., 2000; Cao et al., 2005).

BR is able to enhance seed germination by controlling thenhibitory effects of ABA on seed germination (Finkelstein et al.,008; Zhang et al., 2009). The perception of BR is through BRI1,

leucine receptor similar to a kinase, located on the cell surfaceLi and Chory, 1997). As a result of BR binding to the BRI1 recep-or, phosphorylation of sites changes to the cytosolic domain andKI1 dissociation (the receptor, adversely affecting BR signaling) inhe plasma membrane takes place (He et al., 2000b; Wang et al.,001, 2005; Wang and Chory, 2006). Accordingly, the activation ofRI1 and its interaction with other kinase receptors or other sub-trates results in a set of reactions including the phosphorylationf some plant transcription factors, indicating the level of hormoneignaling (Yin et al., 2002; He et al., 2005; Wang and Chory, 2006).he increase in the rate of the phosphorylation indicates that ABAs able to inhibit BR activity through affecting the related genesZhang et al., 2009).

BR, gibberellic acid and ethylene are able to increase the abi-ty of embryos to grow out of the seed by enhanced rupturingf endosperm and antagonistically interacting with ABA (Finch-avage, Leubner-Metzger, 2006). These hormones are able tonhance seed germination through their own signaling pathway.hile gibberellins and light are able to enhance seed germination

y releasing seed photodormancy, BR can increase seed germina-ion by enhancing the growth of embryo (Leubner-Metzger, 2001).

0. Soil microorganisms and production of plant hormones

Similar to plants, soil microorganisms, including plant growthromoting rhizobacteria (PGPR) such as Azospirillum sp. and Pseu-omonas sp., are also able to produce plant hormones as secondaryetabolites. These hormones are utilized as plant growth promot-

ng substances at the time of inoculating the host plant (Johri,008; Abbas-Zadeh et al., 2009; Jalili et al., 2009). These hormones

nclude auxins, which are produced at levels greater than the otherlant hormones (Zimmer and Bothe, 1988), cytokinins (Cacciarit al., 1989) and gibberellins (Piccoli et al., 1996). It is speculatedhat production of plant hormones may have a prokaryotic origin.

his is because genes are sometimes exchanged between the tworganisms and there is a wide range of microorganisms in the rhi-osphere, which may result in the uptake of DNA by the plant (Bodend Müller, 2003).

xperimental Botany 99 (2014) 110– 121 117

It has been indicated that the production of IAA in the relatedpathway in Azospirillum brasilence is controlled by ipdC gene (VandeBroek et al., 1999; Spaepen et al., 2008), which is expressed inthe stationary growth phase (Vande Broek et al., 2005). The geneipdC, whose crystallographic structure has been recently indicated(Versées et al., 2007a,b), produces phenylpuruvate decarboxylase(Spaepen et al., 2007).

PGPR affect plant growth and soil properties through theiractivities, including the production of plant hormones, enzymes,siderophores, and HCN (Botelho and Mendonc a-Hagler, 2006),resulting in enhanced plant growth and soil structure. For exam-ple, production of 1-amino-1-cyclopropane carboxylic acid (ACC)deminase by Pseudomonas fluorescence and P. putida can enhanceplant growth under a range of stresses. ACC deaminase is able todegrade ethylene, whose production increases under stress andadversely affects plant growth. In addition, such activities alsoresult in enhanced nutrient availability and control of pathogens(Lugtenberg et al., 1991; Nagarajkumar et al., 2004).

The other important and interesting aspect of the effects of soilbacteria on the production of plant hormones is the alteration theymay cause in plant signaling pathways, resulting in the productionof plant hormones by the host plant. Pathogenic bacteria usuallyalter such signaling pathways to their advantage. For example, theAvrB protein in Pseudomonas syringae can increase the host plantsusceptibility to the pathogen by altering the genes related to thejasmonic acid pathway. However, the Arabidopsis protein kinasemap kinase 4 (MPK4) is also necessary for this kind of interaction(Cui et al., 2010; Miransari et al., 2013b).

It is also possible that the production of plant hormones influ-ences symbiotic bacteria, such as nodule N2 fixing bacteria. Duringthe establishment of the soybean (Glycine max L.) and Bradyrhi-zobium japonicum N2-fixing symbiosis the production of planthormones can determine the bacterial population in the nodulesby, for example affecting the available substrate for the use of rhizo-bium (Ikeda et al., 2010). Hormonal interactions between plant andrhizosphere bacteria can affect plant tolerance to stress. As such, theplant and bacteria can be genetically modified so that they can per-form more optimally under a range of conditions, including stress.For example, the gene, which is responsible for the production ofACC-deaminase has been inserted in tomato conferring the plantthe ability to better resist stress (Ghanem et al., 2011).

11. Conclusions and future perspectives

Seed germination and dormancy are important processes affect-ing crop production. These processes are influenced by a rangeof factors, including plant hormones. Plant hormones, producedby both plants and soil bacteria, can significantly affect seed ger-mination. The collection of plant hormones, including ABA, IAA,cytokinins, ethylene, gibberellins and brassinosteroids, can posi-tively or adversely affect seed germination, while interacting witheach other. There are interactions between plant genes and planthormones. Some plant genes, which are necessary for the activ-ity of plant hormones and the other plant genes, are activatedby plant hormones. The molecular pathways, recognized by pro-teomic and molecular biology analyses regarding the perception ofplant hormones, may elucidate more details related to the effects ofplant hormones on seed germination and dormancy. There are alsosome other new interesting finding about seed biology and behav-ior under different conditions. For example, it has been indicatedthat seed activities are regulated by what parts of the seed. More

details related to the hormonal signaling during the growth of plantincluding seed germination have been found. Important role of soilbacteria in the production of plant hormones, and hence seed ger-mination, can be used as a very effective tool for enhanced seed

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ermination, and hence crop production. Future research couldeneficially focus on how the combination of appropriate agricul-ural strategies and biological methods, such as use of soil bacteria,an provide a proper medium for the germination and growth ofeeds under a range of conditions. More details have yet to be indi-ated related to hormonal signaling during seed germination andeed biology. For example, how it is possible to regulate seed ger-ination at dormancy and how the speed of seed germination may

ncrease by adjusting seed behavior under different conditions.

onflict of interest

The authors declare that they do not have any conflict of interest.

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