Plant Hormones and Seed Germination

Home , Cytokinin, Germination, Gibberellin, Phytochrome, Plant hormone, Seed dormancy

Environmental and Experimental Botany 99 (2014) 110–121

Contents lists available at ScienceDirect

Environmental and Experimental Botany

journal homepage: www.elsevier.com/locate/envexpbot

Review

Plant hormones and seed germination

a,b,∗ c

Mohammad Miransari , D.L. Smith

Mehrabad Rudehen, Imam Ali Boulevard, Mahtab Alley, #55, Postal Number: 3978147395, Tehran, Iran

AbtinBerkeh Limited Co., Imam Boulevard, Shariati Boulevard, #107, Postal Number: 3973173831, Rudehen, Tehran, Iran

Plant Science Department, McGill University, 21111 Lakeshore Road, Ste. Anne de Bellevue, Quebec, Canada H9X 3V9

a r t i c l e i n f o a b s t r a c t

Article history: Seed germination is controlled by a number of mechanisms and is necessary for the growth and develop-

Received 5 July 2013

ment of the embryo, resulting in the eventual production of a new plant. Under unfavorable conditions

Received in revised form 1 November 2013

seeds may become dormant (secondary dormancy) to maintain their germination ability. However, when

Accepted 6 November 2013

the 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.

Keywords:

Interactions between plant hormones and plant genes affect seed germination. While the activity of

Plant hormones

plant hormones is controlled by the expression of genes at different levels, there are plant genes that are

Proteomic analysis

activated in the presence of speciﬁc plant hormones. Hence, adjusting gene expression may be an effec-

Seed germination

tive way to enhance seed germination. The hormonal signaling of IAA and gibberellins has been presented

Soil bacteria

as examples during plant growth and development including seed germination. Some interesting results

related 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, as

well as during the establishment of the seedling, by affecting the plant rhizosphere. Most recent ﬁndings

regarding seed germination and dormancy are reviewed. The signiﬁcance of plant hormones including

abscisic acid, ethylene, gibberellins, auxin, cytokinins and brassinosteroids, with reference to proteomic

and molecular biology studies on germination, is also discussed. This review article contains almost a

Contents

1. Introduction ...... 111

2. Seed germination ...... 112

3. Seed dormancy ...... 112

4. ABA ...... 113

5. Ethylene ...... 113

6. Gibberellins ...... 114

7. IAA ...... 115

8. Cytokinins ...... 116

9. Brassinosteroids ...... 117

10. Soil microorganisms and production of plant hormones ...... 117

11. Conclusions and future perspectives ...... 117

Conﬂict of interest ...... 118

References ...... 118

∗

Corresponding author at: Mehrabad Rudehen, Imam Ali Boulevard, Mahtab Alley, #55, Postal Number: 3978147395, Tehran, Iran. Tel.: +98 2176506628;

mobile: +98 9199219047.

E-mail address: [email protected] (M. Miransari).

M. Miransari, D.L. Smith / Environmental and Experimental Botany 99 (2014) 110–121 111

1. Introduction germinates. (1) The sensitivity of seed to ABA and IAA decreases.

The related genes, which are affected, include SNF1-RELATED

Among the most important functions of plant hormones is PROTEIN KINASE2, PROTEIN PHOSPHATASE 2C, LIPID PHOSPHATE

controlling and coordinating cell division, growth and differen- PHOSPHTASE2, ABA INSENSITIVES, and Auxin Response Factor of UBIQ-

tiation (Hooley, 1994). Plant hormones can affect different plant UITIN1 genes. (2) Liu et al. (2013). The inhibiting effects of ABA on

activities including seed dormancy and germination (Graeber seed germination are by adversely affecting the genes of chromatin

et al., 2012). Plant hormones including abscisic acid (ABA), ethyl- assembly and modiﬁcation of cell wall and positively affecting the

ene, gibberellins, auxin (IAA), cytokinins, and brassinosteroids are activity of genes regulating gibberellins catabolic.

biochemical substances controlling many physiological and bio- (1) The decay of seed germination is also related to the IAA

chemical processes in the plant. These interesting products are and jasmonates contents of seed. The following genes are able

produced by plants and also by soil microbes (Finkelstein, 2004; to regulate the jasmonate levels in seed: 3-KETOACYL COENZYME

Jimenez, 2005; Santner et al., 2009). There are hormone recep- A THIOLASE, ALLENE OXIDE SYNTHASE, 12-OXOPHYTODIENOATE

tors with high afﬁnity in the plant, responding to the hormones. REDUCTASE and LIPOXYGENASE. (2) The changes in the expression

Eukaryotes and prokaryotes can utilize similar molecules, which of GA 20-Oxidase and GA 3-Oxidase genes also indicate the likely

act as hormone receptors (Urao et al., 2000; Hwang and Sheen, role of gibberellins in the germination of dormant after-ripening

2001; Mount and Chang, 2002; Santner et al., 2009). seeds (Liu et al., 2013).

Before a seed can germinate a set of stages must be completed, It has been indicated that the activity of the enzyme pectin

including the availability of food stores in the seed. Such food stores methylesterases can affect seed germination. The homogalactur-

include starch, protein, lipid and nutrients, which become avail- onans of the cell wall are methylestriﬁed by the enzyme affecting

able to the seed embryo through the activity of speciﬁc enzymes the cell wall porosity and elasticity and hence cell growth and water

and pathways (Miransari and Smith, 2009). For example, there is uptake. During the process of seed germination the cell wall of the

a group of proteins called cyctatins or phytocyctatins, which are radicle and of the tissues around it must expand. Accordingly, using

able to inhibit the activity of cycteine proteinases as inhibitors a wild and a transgenic type it was indicated that the enzyme can

of protein degradation and regulators during seed germination contribute to the germination of seed by affecting the properties of

(Corre-Menguy et al., 2002; Martinez et al., 2005). the cell wall (Müller et al., 2013).

The whole-genome analyses have indicated the set of genes, The production and activity of plant hormones is controlled

which are related to development, hormonal activity and environ- by the expression level of relevant genes. Accordingly, differences

mental conditions in Arabidopsis. Interestingly, Bassel et al. (2011) in the germination of different seed cultivars are related to their

indicated the distribution of genes in different regions of a seed gene complement. The other important factor that can determine

related to the following processes: (1) dormancy and germination, the expression level of genes in speciﬁc plant tissues is their copy

(2) ripening, (3) ABA activities, (4) gibberellins activities, and (5) number and hence their necessary concentration required for their

stresses such as drought. expression. These kinds of details can be used for the determina-

For example, in region one, seed activity is up or down reg- tion of genes functioning at different plant growth stages, as well

ulated by different genes such as the main dormancy QTL DOG1 as under stress (Miransari, 2012; Miransari et al., 2013a).

and genes, which positively (GID1A and GID1C) or adversely (ABI3, Using microarray analyses Ransom-Hodgkins (2009) recognized

ABI1, ABI5) affect germination. The seed dormancy or germination four genes related to the eukaryotic elongation factor (eEF1A) fam-

is determined by the interactive effects between different signals, ily, which are expressed during the germination of Arabidopsis

such as the germination signals, which promote seed germina- thaliana seeds. These genes are also expressed in the embryos and

tion by inhibiting the activity of signals, which may result in seed the meristems of plant shoots and roots. Inhibiting the expression

dormancy. The network model presented by Bassel et al. (2011) of any one of the four genes resulted in the formation of seedlings

indicates the interactions, which may result in transition from seed with stunted roots and the alteration of expression in the other

dormancy to germination. three genes.

Fu et al. (2005) determined the total number of proteins The protein eEF1A is a multifunctional protein necessary for the

(1100–1300) in the dry and stratiﬁed seeds of Arabidopsis or young following: (1) protein translation, (2) binding actin as well as micro-

seedlings with respect to the time of sampling using gel elec- tubules, (3) bundling actin, and (4) interacting with ubiquitin at

trophoresis. The properties of 437 polypeptides were indicated the time of protein degradation (Ransom-Hodgkins, 2009). There

with the use of mass spectrometric method. Accordingly, the pres- are other functions performed by eEF1A, including a role in the

ence of 293 polypeptides was indicated during all stages, 95 at pathway of various signals, such as phosphatidylinositol 4-kinase

radicle emergence and 18 at the later stages. They also found that (Yang and Boss, 1994), and its role as a substrate for different kinase

226 of polypeptides may be used by different signaling pathways. enzymes (Izawa et al., 2000). This protein can also regulate the

One fourth of proteins were utilized for the metabolism of carbo- activities of the DNA replication/repair protein network (Toueille

hydrate, energy and amino acids, and 3% for the metabolism of et al., 2007) and play a role in apoptosis (Ejiri, 2002). There is a set

vitamins and cofactors. The production of enzymes required for the of 2–15 plant genes producing eEF1A proteins (Aguilar et al., 1991).

genetic processes increased quickly at the beginning of germination There are some photoreceptors that are necessary for plant

and was the highest at 30 h after germination. growth and development, including seed germination. For exam-

Li et al. (2007) investigated also the trend of protein alteration ple, phytochrome B proteins, which are stable and found in green

during different stages of seed germination in four Arabidopsis 12S tissues (Quail, 1997) are able to regulate the hormonal signaling

SSPs. Such kind of analyses can be important for the investigation pathways of auxin and cytokinin (Tian et al., 2002; Fankhauser,

of feeding embryos by the available proteins during germina- 2002; Choi et al., 2005). Phytochromes in the seeds are necessary

tion. Using the two combined methods of 2-DE scheme and mass for controlling seed germination, especially when the seeds are sub-

spectrometry the degradation and accumulation of 12S SSPs were jected to light. Light activates phytochromes, as well as hormonal

evaluated. According to their analyses, 12 SSPs started to accumu- activities in plants (Seo et al., 2009).

late when the process of cell elongation completed in siliques and Different methods have been used for the extraction of

in seeds during their development. bio-chemicals, including plant and bacterial products affecting

According to Liu et al. (2013) the following hormonal and morphological and physiological processes related to seed develop-

signaling processes are likely when a dormant seed (after-ripened) ment. Such discoveries in combination with the use of exogenously

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

applied plant hormones (Lian et al., 2000) have led to more rapid maturation results in inhibition of the cell cycle, decreased seed

advancement of the ﬁeld and some interesting ﬁndings (Miransari moisture, increased ABA levels, production of storage reservoirs

and Smith 2009). Plant hormones are interactive and hence the and established dormancy (Matilla and Matilla-Vazquez, 2008).

production of each may be dependent on the production of other In addition to the effects of plant hormones on seed germination

hormones (Brady et al., 2003; Arteca and Arteca, 2008). researchers have found that both under stress and non-stress con-

There are different parameters affecting the activities of plant ditions, N compounds, including nitrous oxide can enhance seed

hormones including the receptor properties and its afﬁnity for the germination through enhancing amylase activities (Zhang et al.,

hormone, and cytosolic Ca , which, for example, can inﬂuence 2005; Hu et al., 2007; Zheng et al., 2009). Through decreasing

stomatal activities through affecting the K channel (Weyers and the production of O2 and H2O2 such products can also alleviate

Paterson, 2001). Among their other functions, the effects of plant the stress by controlling the likely oxidative damage, similar to

hormones on seed germination may be one of their most important the effects of antioxidant enzymes including superoxide dismutase

functions in plant growth. Hence, in the following such effects are (SOD), catalse (CAT) and peroxidase (POD) on plant growth under

discussed with respect to proteomic and molecular biology studies, various stresses (Song et al., 2006; Tian and Lei, 2006; Tseng et al.,

with a view toward prospects for future research. 2007; Li et al., 2008; Tuna et al., 2008; Zheng et al., 2009; Sajedi

et al., 2011).

In addition, N products can enhance seed germination by

+ +

2. Seed germination adjusting K /Na ratio and increasing ATP production and seed res-

piration (Zheng et al., 2009). The allelopathic effects of seeds can

Seed germination is a mechanism, in which morphological and also positively or adversely affect the germination of their own or

physiological alterations result in activation of the embryo. Before other plant seeds (Ghahari and Miransari, 2009). Proteomic analy-

germination, seed absorbs water, resulting in the expansion and sis of seed germination in Arabidopsis thaliana indicated that during

elongation of seed embryo. When the radicle has grown out of the the process of seed germination 74 proteins are altered before radi-

covering seed layers, the process of seed germination is completed cle emergence and protrusion (Gallardo et al., 2001).

(Hermann et al., 2007). Many researchers have evaluated the pro- Using proteomic analysis it is possible to identify proteins, their

cesses involved in seed germination, and how they are affected by functions and interactions as well as their subcellular localization

plant hormones in a range of plant families, such as the Brassicaceae in a tissue or an organelle. This can be useful for the determina-

(Muller et al., 2006; Hermann et al., 2007). tion of protein alteration during plant development, including the

Seeds contain protein storages, such as globulins and prolamins, formation of speciﬁc tissues and organelles, as well as seed ger-

whose amounts are increased during seed maturation, especially mination. Accordingly, use of proteomics has become increasingly

at the mid- and late-stages of seed maturation, when seeds absorb common in cellular, genetic and physiological research (Pandy and

larger amounts of nitrogen. These proteins are located in the cell Mann, 2000). For example, the proteomic analysis of rice (Oriza

membrane or other parts of the seed. During the time of protein sativa cv Nipponbare) tissues including leaf, root and seed using

translocation into different parts of the seed, negligible amounts of electrophoresis, mass spectrometry and multidimensional protein

protein are turned into other products. The activation of enzymes technology indicated the presence of 2528 unique proteins (Koller

such as proteinase results in the mobilization of storage proteins et al., 2002).

(Wilson, 1986).

Storage proteins are also found in the seedling radicle and shoot

(Tiedemann et al., 2000). The mobilization of storage proteins does 3. Seed dormancy

not take place at the same time in different parts of the seed. The

other enzymes, which are activated during the mobilization of pro- Seed dormancy is a mechanism by which seeds can inhibit

teins, are carboxypeptidase and aminopeptidase. Among the most their germination in order to wait for more favorable conditions

important parameters controlling the process of seed dormancy (secondary dormancy) (Finkelstein et al., 2008). However, primary

are changes at molecular levels, including the protein and hor- dormancy is caused by the effects of abscisic acid during seed devel-

monal alterations, and the balance between ABA and gibberellins opment. Such seeds may never germinate (Bewley, 1997). Usually

(Ali-Rachedi et al., 2004; Finch-Savage and Leubner-Metzger 2006; freshly harvested seeds of plants like barley (Hordeum vulgare L.) are

◦

Finkelstein et al., 2008; Graeber et al., 2010). Parameters such as the not able to germinate at temperatures higher than 20 C (Corbineau

related genes, chromatin related factors, and the processes, which and Come, 1996; Leymarie et al., 2007). In barley the process of

are non-enzymatic, affect seed dormancy. The genes, which control dormancy is due to the ﬁxation of oxygen by glumellae during the

dormancy, include the maturating genes, hormonal and epigenetic oxidation of phenolic products, resulting in the limitation of oxygen

regulating genes, and the genes, which control release from dor- supplement to the embryo. The resulting hypoxia may also inter-

mancy (Graeber et al., 2012). fere with ABA activities in the seed (Benech-Arnold et al., 2006).

Use of mutants is one of the most interesting ways to deter- Gibberellins are able to activate dormant seeds, although the

mine the role of each plant hormone, in seed germination. The hormone does not control seed dormancy (Bewley, 1997; Miransari

synthesis of DNA and mitotic microtubules are among the vari- and Smith, 2009). ABA can inhibit corn germination by affecting the

ous changes taking place during embryogenesis, and these can be cell cycle. This is the reason for the more rapid germination of seeds

used as the indicators of cell division and differentiation during that are deﬁcient in ABA. Inhibition of the cell cycle by ABA is related

this stage. These processes are paralleled by seed abilities to toler- to activation of a residual G1 kinase, which becomes inactivated in

ate desiccation and become dormant (Finkelstein, 2004; de Castro the absence of ABA (Sanchez et al., 2005).

and Hilhorst, 2006). By affecting hormonal balance in the seed, environmental

Seed development includes the formation of the embryo body parameters including salinity, acidity, temperature and light, can

by cell division and differentiation, resulting in the formation of inﬂuence seed germination (Ali-Rachedi et al., 2004; Alboresi et al.,

−

embryonic organs (Goldberg et al., 1994; Meinke, 1995). This period 2006). Nitrate (NO3 ) and gibberellins are able to enhance seed

−

covers the maturation of seed, including the formation of organs germination. NO3 can act as a source of N and a seed germina-

and nutrient storage, as well as changes in the embryo size and tion enhancer. Similarly, gibberellins enhance seed germination by

weight, followed by the acquisition of desiccation tolerance and inhibiting ABA activity. It is caused by the activation of catabolyzing

dormancy (Finkelstein, 2004; de Castro and Hilhorst, 2006). Seed enzymes and inhibition of the related biosynthesis pathways,

M. Miransari, D.L. Smith / Environmental and Experimental Botany 99 (2014) 110–121 113

which also decreases ABA amounts (Toyomasu et al., 1994; Atia 2001), indicating that sometimes the appoplasm may be the impor-

et al., 2009). Enzymes including nitrite reductase, nitrate reduc- tant compartment. Soluble factors, F-box proteins, are receptors for

−

tase, and glutamine synthetase assimilate NO3 into amino acids IAA (Dharmasiri et al., 2005a,b; Kepinski and Leyser, 2005; Santner

and proteins. et al., 2009). For ABA, one family of proteins called PYR/PYL/PAR

Salinity decreases seed germination by affecting the seed nitro- is the receptor (Park et al., 2009). IAA is the most important hor-

gen (N) content and hence embryo growth. This indicates how N mone for the process of somatic embryogenesis (Cooke et al., 1993;

compounds can alleviate the stress of salinity on seed germination Jimenez, 2005). Researchers have recently found two new G pro-

(Atia et al., 2009). N can also inhibit seed dormancy by decreasing teins, which are ABA receptors (Pandey et al., 2009).

the level of ABA in the seed (Ali-Rachedi et al., 2004; Finkelstein The role of ABA and its responsive genes in the process of

et al., 2008). The unfavorable effects of salinity on seed germina- seed germination has been indicated (Nakashima et al., 2006;

tion include: (1) decreasing the amounts of seed enhancer products Graeber et al., 2010). The inhibitory effects of ABA on seed ger-

−

including NO3 and gibberellins, (2) enhancing ABA amounts, and mination is through delaying the radicle expansion and weakening

(3) altering membrane permeability and water behavior in the seed of endosperm, as well as the enhanced expression of transcription

(Khan and Ungar, 2002; Lee and Luan, 2012). factors, which may adversely affect the process of seed germina-

ABA and gibberellins are necessary for dormancy initiation and tion (Graeber et al., 2010). The gibberrelin repressor RGL2 is able to

seed germination, respectively (Groot and Karssen, 1992; Matilla inhibit seed germination by stimulating the production of ABA as

and Matilla-Vazquez, 2008). The gibberellins/ABA balance deter- well as the related transcription factors (Piskurewicz et al., 2008).

mines seed ability to germinate or the pathways necessary for seed The H subunit of a chloroplast protein, Mg-chelatase can act as ABA

maturation (White et al., 2000; White and Rivin, 2000; Chibani receptor during different growth stages of plant including seed ger-

et al., 2006; Finch-Savage and Leubner-Metzger, 2006). While mination (Shen et al., 2006). It has recently been suggested that

ABA determines seed dormancy and inhibits seed from germina- GPROTEIN COUPLED RECEPTOR 2 can also act as another ABA recep-

tion, gibberellins are necessary for seed germination (Matilla and tor, mediating different activities of ABA, including its effects on

Matilla-Vazquez, 2008). seed germination (Liu et al., 2007b). However, other researchers

Although seed dormancy is under the inﬂuence of plant hor- indicated that such a receptor is not necessary for activities medi-

mones, seed morphological and structural characteristics such as ated by ABA, including the process of seed germination (Johnston

endosperm, pericarp and seed coat properties can also affect seed et al., 2007; Guo et al., 2008).

dormancy (Kucera et al., 2005). Both ethylene and gibberellins

affect radicle growth, with gibberellins being the most important

hormone. Although gibberellins are necessary for the production 5. Ethylene

of mannanase, which is necessary for seed germination, ethyl-

ene is not (Wang et al., 2005a,b). However, in gibberellin deﬁcient Compared with the other plant hormones, ethylene has the sim-

mutants, ethylene can act similar to gibberellins, because the seeds plest biochemical structure. However, it can inﬂuence a wide range

are able to germinate completely in such a situation (Karssen et al., of plant activities (Arteca and Arteca, 2008). Similar to cytokinin,

1989; Matilla and Matilla-Vazquez 2008). the perception of ethylene is by a kinase receptor, which is a two-

Using proteomic analyses the molecular and biological stages component protein. However, for ethylene the receptor is located

related to seed germination have been elucidated. At different in the membrane of endoplasmic reticulum (Kendrick and Chang,

stages of seed germination, expression of different genes results 2008; Santner et al., 2009). Although ethylene can affect differ-

in the production of proteins, necessary for seed germination and ent plant activities, including tissue growth and development, and

dormancy release. Proteins necessary for seed germination are seed germination, however it is not yet understood how ethylene

accumulated after-ripening, under seed drying conditions, result- inﬂuences seed germination. There are different ideas regarding

ing in the release of dormancy (Gallardo et al., 2001; Chibani et al., seed germination; according to some researchers ethylene is pro-

2006). duced as a result of seed germination and according to the other

researchers ethylene is necessary for the process of seed germina-

tion (Matilla, 2000; Petruzzelli et al., 2000; Rinaldi, 2000).

4. ABA Ethylene is able to regulate plant responses, under a range

of conditions, including stress. For example, in combination with

While ABA positively affects stomatal activity, seed dormancy ABA, ethylene is able to affect plant response to salinity. Under

and plant activities under stresses such as ﬂooding (abiotic) and increased levels of salinity, ethylene production in plants increases,

pathogen presence (biotic) (Moore, 1989; Davies and Jones, 1991; which decreases plant growth and development. The enzyme 1-

Weyers and Paterson 2001; Popko et al., 2010), it adversely affects aminocyclopropane-1 carboxylic acid (ACC) is a pre-requisite for

the process of seed germination. For example, concentrations of ethylene production, catalyzed by ACC oxidase. During the time

1–10 ␮M can inhibit seed germination in plants like Arabidopsis that seed is exposed to the stress, ethylene production is affected

thaliana (Kucera et al., 2005; Muller et al., 2006). However, other (Mayak et al., 2004; Jalili et al., 2009).

plant hormones including gibberellins, ethylene, cytokinins, and The amount of ethylene increases during the germination of

brassinosteroids, as well as their negative interaction with ABA, can many plant seeds including wheat, corn, soybean and rice, affecting

positively regulate the process of seed germination (Kucera et al., the rate of seed germination (Pennazio and Roggero, 1991; Zapata

2005; Hermann et al., 2007). Under stress ABA can be quickly pro- et al., 2004). ACC can enhance seed radicle emergence through the

duced as a ␤-glucosidase (Lee et al., 2006). Additionally, it has been production of ethylene, produced in the radicle (Petruzzelli et al.,

indicated that phosphatase regulators can also act as ABA receptors 2000, 2003). With respect to the easy production of ethylene from

(Ma et al., 2009). ACC in the presence of ACC oxidase, ACC has been widely tested in

The movement of ABA across the cellular membrane is under numerous experiments (Petruzzelli et al., 2000; Kucera et al., 2005).

the inﬂuence of pH and cellular compartment. Hence, it is likely It has been indicated that during the ﬁnal stage of seed ger-

to predict the hormone concentration in different cellular com- mination ethylene is produced in different plant species and

partments, according to its cellular pH and compartment. Different it can contribute to the germination of seeds after dormancy.

experiments have demonstrated that the receptors for ABA and IAA Ethylene is produced through the pathway that turns S-adenosyl-

are located outside the plasma membrane (Weyers and Paterson, Met into 1-Amicocyclopropane-1-carboxillic-acid (ACC) by ACC

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

Fig. 1. (A) Interactions between GID1 and DELLA proteins, which result in the eventual recognition of DELLA proteins, and hence the lifting of gibberellins DELLA repression.

(B) However, in a mutant, the formation of GID1-GA-DELLA complex inhibits the lifting of DELLA repression. (C) DELLA phosphorylation adversely affects DELLA responding.

(Redrawn) (Hauvermale et al., 2012a,b; with kind permission, # 3218660692166, from American Society of Plant Physiologists; American Society of Plant Biologists).

synthase, followed by the oxidation of ACC to ethylene by ACC oxi- enzymes can degrade seed proteins during the ﬁrst stages of ger-

dase (Yang and Hoffman, 1984; Kende, 1993; Argueso et al., 2007). mination.

The amounts of ethylene increase under stress and it can control The novel mechanism by which ethylene inhibits the adverse

numerous processes in plants, including ﬂowering, fruit ripening, effects of ABA on the release of seed dormancy has been attributed

aging, dormancy inhibition and seed germination (Matilla, 2000; to the production of OH in the apoplasm. Production of reactive

Nath et al., 2006; Matilla and Matilla-Vazquez, 2008). oxygen species in the apoplasm can also affect seed germination

As previously mentioned, ethylene is also important during (Chen, 2008; Muller et al., 2009; Graeber et al., 2010). Reactive

stress and its production and hence plant growth is affected oxygen species are produced at different stages of seed growth

(Druege, 2006). Researchers have indicated that ethylene in plants and development. Usually reactive oxygen species adversely affect

increases under stress, which can decrease plant growth, includ- seed activities. However, some new ﬁndings indicate that there are

ing that of plant roots. Interestingly, they have also found that the also some positive effects for reactive oxygen species, including

bacterial enzyme ACC deaminase is able to alleviate such stresses the germination of seeds and the growth of seedlings by the reg-

by degrading the ethylene pre-requisite ACC (Mayak et al., 2004). ulation of cell growth and development, as well as by controlling

Ethylene can also inﬂuence plant performance by affecting the pathogens and cell redox conditions. Reactive oxygen species may

production and functioning of other hormones, for example by also positively affect the release of seed dormancy by interacting

affecting the related pathways (Arora, 2005; Vandendussche and with gibberellin and abscisic acid transduction pathways, affect-

Van Der Straeten, 2007). ing many transcriptional factors and proteins (El-Maarouf-Bouteau

The membrane localized receptors of Arabidopsis, which are and Bailly, 2008).

necessary for the perception of ethylene are activated by several

genes including ETR1, ERS1, ETR2, ERS2 and EIN4 with the follow- 6. Gibberellins

ing domains: (1) N-terminal for biding ethylene, (2) C-terminal

receiver (not present in the ERS1 and ERS2 genes) and (3) histi- Gibberellins are diterpenoid, regulating plant growth. They are

dine protein kinase. As a result of ethylene binding such receptors commonly used in modern agriculture and were ﬁrst isolated from

become inactive (Gallie and Young, 2004). However, only two of the metabolite products of the rice pathogenic fungus, Gibberella

such genes are necessary for the activation of maize localized- fujikuroi, in 1938 (Yamaguchi 2008; Santner et al., 2009). The

membrane receptors as well as for the activation of ACC synthase biosynthesis of gibberellins is from geranyldiphosphate through

and ACC oxidase, for example in the endosperm and embryo. The a pathway including several enzymes. Gibberellins are adversely

high expression of ethylene receptors in the embryo can enable the regulated by DELLA proteins, with a C-terminal GRAS domain in

embryo to grow. their structure, which are eventually degraded by the E3 ubiquitin

Brassinosteroids (BR) and IAA are able to stimulate the produc- ligase SCF (GID2/SLY1) (Itoh et al., 2003; Schwechheimer 2008).

tion of ethylene (Arteca and Arteca, 2008). Gibberellins, ethylene Accumulation of DELLAs in seeds can result in the expres-

and BR can induce seed germination by rupturing testa and sion of genes producing F-box proteins. The gibberellins receptor

endosperm, while antagonistically interacting with the inhibitory has recently been identiﬁed in rice. It is GIBBERELLINE INSEN-

effects of ABA on seed germination (Finch-Savage and Leubner- STIVE DAWRF1 (GID1) protein (interacting with DELLA proteins

Metzger, 2006; Holdsworth et al., 2008; Finkelstein et al., 2008). and resulting in their eventual degradation) located in the nucleus,

Ethylene is able to make dormant seeds germinate. It has been and can bind to the gibberellins, which are biologically active (Fig. 1)

suggested that by regulating the expression of cysteine-proteinase (Ueguchi-Tanaka et al., 2005; Grifﬁths et al., 2006; Nakajima et al.,

genes, and its protein complex, proteasome, ethylene can remove 2006; Willige et al., 2007). Through its antagonistic effects with

seed dormancy (Asano et al., 1999; Borghetti et al., 2002). These ABA, gibberellins, which are internal signals, are able to release

M. Miransari, D.L. Smith / Environmental and Experimental Botany 99 (2014) 110–121 115

seeds from dormancy (Gubler et al., 2008; Seo et al., 2009). In Ara- (with about 4000 genes), Yang et al. (2004) identiﬁed some rice seed

bidopsis thaliana the three receptors, GID1a, GID2b, and GID2c act genes, regulated by gibberellins and brassinosteroids. However,

as gibberellins receptors. The weakening of endosperm is by the to identify more gibberellins and brassinosteroids related genes

activation of gibberellins genes affecting the modifying proteins use of cDNA, with more genes as well as use of mutants is nec-

of cell wall (Voegele et al., 2011). However, ABA can prevent the essary. This kind of analysis may result in more details regarding

weakening of endosperm (Muller et al., 2006; Linkies et al., 2009). the activity and role of the hormones. The important point, which

The seed endosperm, which becomes available to the embryo, must be indicated about gibberellins, is to indicate if DELLA ability

through the activities of some hydrolase enzymes, is made of the to bind to GID1 or other proteins can be inﬂuenced by modifying

starchy part of the seed and the surrounding aleurone (Jones and posttranscriptional. DELLA controlling of plant development is by

Jacobsen, 1991; Bosnes et al., 1992). Gibberellins stimulate the ZIM domain control JAZ1 and bHLH and GRAS transcription factors

synthesis and production of the hydrolases, especially ␣-amylase, (Hauvermale et al., 2012a,b).

resulting in the germination of seeds. Gibberellins are able to induce

a range of genes, which are necessary for the production of amy-

lases including ␣-amylase, proteases and ␤-glucanases (Appleford 7. IAA

and Lenton, 1997; Yamaguchi, 2008). Different processes in the

seed indicate that seed aleurone is appropriate for the evaluation Auxin is a plant hormone, which plays a key role in regulating

of transduction pathways at the time of plant hormones produc- the following functions: cell cycling, growth and development, for-

tion, including gibberellins (Ritchie and Gilroy, 1998; Penﬁeld et al., mation of vascular tissues (Davies, 1995) and pollen (Ni et al., 2002),

2005; Achard et al., 2008; Schwechheimer, 2008). and development of other plant parts (He et al., 2000a). The growth

The plant hormone gibberellins are necessary for seed germi- and development of different plant parts, including the embryo,

nation. The Signaling pathways of hormone can stimulate seed leaf and root is believed to be controlled by auxin transport (Liu

germination through the release of coat dormancy, “weakening of et al., 1993; Xu and Ni, 1999; Rashotte et al., 2000; Benjamins and

endosperm”, and “expansion of embryo cell”. Proteins resulting Scheres, 2008; Popko et al., 2010). Such kind of regulation is by

in the modiﬁcation of cell wall like xyloglucan endotransglyco- affecting the transcriptional factors (Hayashi, 2012).

sylase/hydrolases (XTHs) and expansins may enhance the above Auxin is bound to AFB receptors as the subunits of ligase com-

mentioned pathways (Liu et al., 2005; Voegele et al., 2011). The plex of SCF ubiquitin. The speciﬁcity of auxin regulated genes is

interesting mechanism, which controls seed germination, is the determined by the following: the related proteins, the regulation

suppressing effects of excess ABA on embryo expansion, which of their post transcripts, their related stability and the afﬁnity

inhibit the promoting effects of gibberellins on radicle growth, between the related proteins. The protein ABP1 is the auxin bind-

and hence it will not germinate through the endosperm and testa ing protein, which can act as a receptor in the non- transcriptional

(Nonogaki, 2008). signaling of auxin. ABP1 is also able to mediate the genes regulat-

It has been indicated that there is an intimate interaction ing the activity of AFB receptors. Hence, both ABP1 and AFB are able

between gibberellins metabolism and gibberellins response path- to regulate the physiological activities of auxin. Another important

ways. This kind of interaction, along with other pathways in the function deﬁned for auxin is elongation of cell, which is done non-

plant, results in the regulation of plant growth and development. transcriptionally with the help of ABP1 activating the expression

Using proteomic analysis Gallardo et al. (2002) indicated the way of AUX/IAAs genes. Such kind of receptors regulates the signaling

via which the germination of Arabidopsis seeds is regulated by gib- responses of auxin during cell cycling. Gibberellins can also simi-

berellins. In this kind of interaction, the ␣-tublin a component of larly affect cell cycling in plant (Hauvermale et al., 2012a,b).

the cytoskeleton is affected by the hormone. Auxin by itself is not a necessary hormone for seed germina-

Expression of the Osem gene is regulated by gibberellins as well tion. However, according to the analyses regarding the expression

as by ABA. This gene is homologous to the Em gene of wheat, of auxin related genes, auxin is present in the seed radicle tip dur-

which regulates the production of one of the embryogenesis abun- ing and after seed germination. In addition, microRNA60 inhibits

dant proteins. Gibberellins are able to inﬂuence leaf growth by auxin RESPONSE FACTOR10 during seed germination so that the

regulating the activity of lactoylglutathione lyase (Hattori et al., seed can germinate. Such a controlling process is also neces-

1995). Gibberellins upregulation of photosystem II oxygen produc- sary for the stages related to post-emergence growth, including

tion may enhance the efﬁciency of energy pathways in plant tissues. seed maturation. The mechanisms for such inhibitory effects have

This may also be the case in germinating seedlings (Finkelstein et al., been attributed to interactions with the ABA pathway (Liu et al.,

2002). 2007a, b). Although IAA may not be necessary for seed germina-

Gibberellins are also able to regulate the activity of RPA1 (repli- tion, it is necessary for the growth of young seedlings (Bialek et al.,

cation protein A1) gene, which are found in signiﬁcant amounts 1992; Hentrich et al., 2013). The accumulated IAA in the seed cotyle-

in tissues with actively dividing cells (Van der Knaap et al., 2000), don is the major source of IAA for the seedlings. In legumes, amide

as well as the activity of plant receptors, such as kinases. In addi- products are the major source of IAA in mature seeds (Epstein et al.,

tion, gibberellins can inﬂuence the production of proteins during 1986; Bialek and Cohen, 1989).

pathogenic, oxidative and heavy metal stress (Marrs, 1996). There are some AUXIN RESPONSE FACTORS acting as tran-

The regulation of proteins, with a range of functions, in cul- scription factors and controlling different stages of plant growth

tured cells by gibberellins is also of signiﬁcance. These proteins and development. For example, in Arabidopsis thaliana such genes

include the ones regulating metabolism (formate dehydrogenase), are inﬂuenced by microRNA’s, which are small (with 21–24

transcription (nucleotide binding proteins), protein folding (chap- nucleotides) single stranded RNA’s, affecting gene activity at post-

eronins), energy (GADPH), signal transduction (G proteins), and transcriptional level (Bartel, 2004). Among the most important

cell growth (GF14-c protein) (Olszewski et al., 2002). Plant growth effects of microRNA’s are the followings: (1) plant growth, (2)

and development is signiﬁcantly affected by the cross talk between hormonal signaling, (3) homeostasis and (4) responses to environ-

plant hormones (Davies, 1995). The activity of plant genes is usu- mental and nutritional alterations (Juarez et al., 2004; Liu et al.,

ally regulated by more than one plant hormone (Yang et al., 2004; 2007a, b). MicroRNA’s are able to regulate a number of hormonal

Depuydt and Hardtke, 2011). transduction pathways.

The activity of genes regulated by gibberellins is adversely For example, the activity of gibberellins is regulated by

affected by ABA. In their research, constructing a cDNA microarray microRNA’s in the presence of DELLA proteins. During the

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

regulation of auxin activity (its signal transduction pathway) by through the activity of a phosphoribohydrolase enzyme, turning

microRNA’s, auxin binds its receptor, which is an F-box protein the nucleotide into a free base (Santner et al., 2009).

and proteolyses the AUX/IAA proteins. These proteins interact Signaling in cytokinins is very similar to the two-component

with ARFs by binding the auxin response elements and activate signaling in the bacterial species (To and Kieber 2008). In this

or repress the activity of the related genes (Ulmasov et al., 1997, kind of perception, the initiation of phosphorelay by ligand bind-

1999). ing is related to kinases histidine and asparate. The perceiving

Researchers have successfully used microRNA-resistant compounds, which are in nucleus, are able to phosphorylate the

mutants to determine how ARFs may function biologically. They response proteins, which can negatively or positively regulate

found that the down regulation of these ARF’s is necessary for cytokinin signaling. Similar to auxin, cytokinins are also able to

the growth and development of root, leaf and ﬂower. Using seed regulate many genes, including CYTOKININ RESPONSE FACTORS

and seedling of mutants, the important role of auxin signaling (Rashotte et al., 2003; Santner et al., 2009).

pathways during the ﬁrst stages of seedling development was The cytokinin receptors (Arabidopsis thaliana) are able to regu-

determined. The importance of microRNA’s and ARF’s affecting late different functions related to the development and physiology

the interaction of auxin and ABA during the stages of germination of Arabidopsis thaliana. They include AHK2, AHK3 and CRE1/AHK4

and post germination was clariﬁed (Liu et al., 2007a, b). Mutation with the following activities. (1) Embryo development by affect-

in some of genes, such as ibr5 (indole-3-butyric acid-response ing the cellular division, which subsequently causes the vesicular

5), with some similarity to MAPK (mitogen-activated protein to differentiate, (2) seed size, (3) seed production and germina-

kinase) phosphatases decreases their sensitivity to auxin as well tion, (4) hypocotyls and shoot growth, (5) senescence of leaf, (6)

as the response of roots to ABA, and increases the rate of seed root growth, (7) nutrient uptake, (8) handling stress (Rieﬂer et al.,

germination in the presence of ABA (Monroe-Augustus et al., 2006; Heyl et al., 2012). However, in the other plants the functions

2003). of cytokinin receptors (MtCRE1, LjCRE1, LaHK1, MsHK1, and BpCRE1

Accordingly, the adverse effects of microRNA160 on ARF10 can PtCRE1) include: (1) root production and growth, (2) symbiosis pro-

affect the processes of seed germination and post germination (Liu cess, (3) formation of root nodules, and (4) nodule senescence (Coba

et al., 2007a, b). In transgenic plants the resistance of ARF10, versus de la Pena et al., 2008a,b; Heyl et al., 2012).

microRNA activity may result in growth defects of some plant parts The following indicates the interactions, which may exist

including leaf, ﬂower and stem. The ARF10 mutant plants indicate between the cytokinin receptor and the related ligand. (1) There

a high level of sensitivity to ABA. Similarly, exogenous IAA can also is a high afﬁnity between cytokinin receptors and most natural

result in such responses by a wild-type plant. However, it is likely cytokinins, which are active, (2) the receptors has only one site

to decrease seed sensitivity to ABA by overexpressing microRNAs for ligand binding, (3) the afﬁnity of cytokinin receptors to the dif-

(Liu et al., 2007a, b). ferent cytokinins is determined by their activities in the bioassays,

The most important plant hormones for seed germination are (4) cytokinin can ﬁrmly bind over a wide range of conditions, (5)

ABA and gibberellines, which have inhibitory and stimulatory the cytokinin receptors of Arabidopsis thaliana and maize indicate

effects on seed germination, respectively. BR and ethylene also have similar properties (Heyl et al., 2012).

enhancing effects on seed germination. Although IAA by itself may Although there is some ﬁnding about cytokinin receptors, there

not be important for seed germination, its interactions and cross are yet more to be learnt regarding cytokinin receptors. The details

talk with gibberellins and ethylene may inﬂuence the processes regarding the three dimensional structure of the receptor domain

of seed germination and establishment (Fu and Harberd, 2003; and its related evolution may signiﬁcantly indicate some important

Chiwocha et al., 2005). and new details related to the action of cytokinin receptors. For

Alteration of the auxin signaling pathway, by altering auxin example, how the receptors may transfer signal from and across

response factor, increases seed sensitivity to ABA, as mRNA60 may the membrane to the cytoplasm. Considering plant shoot and root,

affect the ABA responsive gene by repressing auxin response fac- as the action sites of receptors, it must be yet indicated which

tor (Liu et al., 2007a, b). Auxin can inﬂuence seed germination, activities of cytokinins are regulated by their receptors (Heyl et al.,

when ABA is present (Brady et al., 2003). Accordingly, mRNA60 is 2012).

able to regulate the cross-talk between IAA and ABA. However, the Cytokinins are also able to enhance seed germination by the

molecular mechanism regulating the interactions and cross-talk alleviation of stresses such as salinity, drought, heavy metals and

between IAA and ABA is not known yet. IAA is also able to affect oxidative stress (Khan and Ungar, 1997; Atici et al., 2005; Nikolic

seed germination by affecting the activity of enzymes for example, et al., 2006; Peleg and Blumwald, 2011). They can be inactivated

in germinating pea seeds, the activity of glyoxalase I was regulated by the enzyme cytokinin oxidase/dehydrogenase (Galuszka et al.,

by IAA, resulting in higher rates of cell growth and development 2001) catalyzing the cleavage of their unsaturated bond. Different

(Thornalley, 1990; Hentrich et al., 2013). activities 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).

8. Cytokinins Arabidopsis thaliana has three histidine kinases that can act as

receptors for cytokinins (Inoue et al., 2001; Yamada et al., 2001).

Cytokinins are derived from adenine molecules in which there Controlling seed size, including embryo, endosperm and seed coat

is a side chain at the N6 position. Miller was the ﬁrst to dis- growth, is also among the functions of cytokinins. Endosperm and

cover them, in the 1950s, based on their ability to enhance plant seed coat growth in Arabidopsis is followed by embryo growth, at

cell division (Miller et al., 1955). Cytokinins are plant hormones, a later stage of embryogenesis, which is less related to the ﬁnal

regulating a range of plant activities including seed germination. seed size (Mansﬁeld and Bowman, 1993). There are several factors

They are active in all stages of germination (Chiwocha et al., 2005; controlling seed number with respect to the number of seeds, and

Nikolic et al., 2006; Rieﬂer et al., 2006). They can also affect the the most important of these is the available carbon source for seed

activities of meristemic cells in roots and shoots, as well as leaf utilization (Rieﬂer et al., 2006).

senescence. In addition, they are effective in nodule formation dur- Subbiah and Reddy (2010) investigated the interactive effects

ing establishment of the N2-ﬁxing symbiosis and other interactions of different plant hormones on seed germination in an ethylene-

between plant and microbes (Murray et al., 2007; To and Kieber, related mutated Arabidopsis. The mutation of etr1 and ein2

2008; Santner et al., 2009). The production of active cytokinins is genes, which adversely affects the ethylene response, resulted in

M. Miransari, D.L. Smith / Environmental and Experimental Botany 99 (2014) 110–121 117

enhanced seed dormancy and delayed seed germination related to It has been indicated that the production of IAA in the related

the wild type. Mutated etr1, ein2 and ein6 also resulted in enhanced pathway in Azospirillum brasilence is controlled by ipdC gene (Vande

response to ABA with respect to its inhibitory effects on seed Broek et al., 1999; Spaepen et al., 2008), which is expressed in

germination. However, mutation of ctr1 and eto3 genes, which sig- the stationary growth phase (Vande Broek et al., 2005). The gene

niﬁcantly enhance ethylene response and production, decreased ipdC, whose crystallographic structure has been recently indicated

seed sensitivity to ABA at germination. Use of AgNO3 also increased (Versées et al., 2007a,b), produces phenylpuruvate decarboxylase

sensitivity to ABA during germination through its inhibitory (Spaepen et al., 2007).

effects on ethylene activity. However, addition of cytokinin N-6 PGPR affect plant growth and soil properties through their

benzyl adenine (BA) decreased the enhanced response of ethylene- activities, including the production of plant hormones, enzymes,

resistant mutants to ABA, indicating that not all effects of cytokinin siderophores, and HCN (Botelho and Mendonc¸ a-Hagler, 2006),

on seed germination are through its effects on ethylene activity. 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 enhance

9. Brassinosteroids plant growth under a range of stresses. ACC deaminase is able to

degrade ethylene, whose production increases under stress and

Brassinosteroids (BR) are a class of plant hormones, similar to adversely affects plant growth. In addition, such activities also

the steroid hormones in other organisms (Rao et al., 2002; Bhardwaj result in enhanced nutrient availability and control of pathogens

et al., 2006; Arora et al., 2008). The cholestane hydroxylated deriva- (Lugtenberg et al., 1991; Nagarajkumar et al., 2004).

tives produce BR and the C-17 side chain and rings and the related The other important and interesting aspect of the effects of soil

replacements determine the variations in the hormonal structure bacteria on the production of plant hormones is the alteration they

(Arora et al., 2008). BR has a wide range of activities in plant growth may cause in plant signaling pathways, resulting in the production

and development including cell growth, vascular formation, repro- of plant hormones by the host plant. Pathogenic bacteria usually

ductive growth, seed germination, and production of ﬂowers and alter such signaling pathways to their advantage. For example, the

fruit (Khripach et al., 2000; Cao et al., 2005). AvrB protein in Pseudomonas syringae can increase the host plant

BR is able to enhance seed germination by controlling the susceptibility to the pathogen by altering the genes related to the

inhibitory effects of ABA on seed germination (Finkelstein et al., jasmonic acid pathway. However, the Arabidopsis protein kinase

2008; Zhang et al., 2009). The perception of BR is through BRI1, map kinase 4 (MPK4) is also necessary for this kind of interaction

a leucine receptor similar to a kinase, located on the cell surface (Cui et al., 2010; Miransari et al., 2013b).

(Li and Chory, 1997). As a result of BR binding to the BRI1 recep- It is also possible that the production of plant hormones inﬂu-

tor, phosphorylation of sites changes to the cytosolic domain and ences symbiotic bacteria, such as nodule N2 ﬁxing bacteria. During

BKI1 dissociation (the receptor, adversely affecting BR signaling) in the establishment of the soybean (Glycine max L.) and Bradyrhi-

the plasma membrane takes place (He et al., 2000b; Wang et al., zobium japonicum N2-ﬁxing symbiosis the production of plant

2001, 2005; Wang and Chory, 2006). Accordingly, the activation of hormones can determine the bacterial population in the nodules

BRI1 and its interaction with other kinase receptors or other sub- by, for example affecting the available substrate for the use of rhizo-

strates results in a set of reactions including the phosphorylation bium (Ikeda et al., 2010). Hormonal interactions between plant and

of some plant transcription factors, indicating the level of hormone rhizosphere bacteria can affect plant tolerance to stress. As such, the

signaling (Yin et al., 2002; He et al., 2005; Wang and Chory, 2006). plant and bacteria can be genetically modiﬁed so that they can per-

The increase in the rate of the phosphorylation indicates that ABA form more optimally under a range of conditions, including stress.

is able to inhibit BR activity through affecting the related genes For example, the gene, which is responsible for the production of

(Zhang et al., 2009). ACC-deaminase has been inserted in tomato conferring the plant

BR, gibberellic acid and ethylene are able to increase the abi- the ability to better resist stress (Ghanem et al., 2011).

ity of embryos to grow out of the seed by enhanced rupturing

of endosperm and antagonistically interacting with ABA (Finch-

Savage, Leubner-Metzger, 2006). These hormones are able to 11. Conclusions and future perspectives

enhance seed germination through their own signaling pathway.

While gibberellins and light are able to enhance seed germination Seed germination and dormancy are important processes affect-

by releasing seed photodormancy, BR can increase seed germina- ing crop production. These processes are inﬂuenced by a range

tion by enhancing the growth of embryo (Leubner-Metzger, 2001). of factors, including plant hormones. Plant hormones, produced

by both plants and soil bacteria, can signiﬁcantly affect seed ger-

mination. The collection of plant hormones, including ABA, IAA,

10. Soil microorganisms and production of plant hormones cytokinins, ethylene, gibberellins and brassinosteroids, can posi-

tively or adversely affect seed germination, while interacting with

Similar to plants, soil microorganisms, including plant growth each other. There are interactions between plant genes and plant

promoting rhizobacteria (PGPR) such as Azospirillum sp. and Pseu- hormones. Some plant genes, which are necessary for the activ-

domonas sp., are also able to produce plant hormones as secondary ity of plant hormones and the other plant genes, are activated

metabolites. These hormones are utilized as plant growth promot- by plant hormones. The molecular pathways, recognized by pro-

ing substances at the time of inoculating the host plant (Johri, teomic and molecular biology analyses regarding the perception of

2008; Abbas-Zadeh et al., 2009; Jalili et al., 2009). These hormones plant hormones, may elucidate more details related to the effects of

include auxins, which are produced at levels greater than the other plant hormones on seed germination and dormancy. There are also

plant hormones (Zimmer and Bothe, 1988), cytokinins (Cacciari some other new interesting ﬁnding about seed biology and behav-

et al., 1989) and gibberellins (Piccoli et al., 1996). It is speculated ior under different conditions. For example, it has been indicated

that production of plant hormones may have a prokaryotic origin. that seed activities are regulated by what parts of the seed. More

This is because genes are sometimes exchanged between the two details related to the hormonal signaling during the growth of plant

organisms and there is a wide range of microorganisms in the rhi- including seed germination have been found. Important role of soil

zosphere, which may result in the uptake of DNA by the plant (Bode bacteria in the production of plant hormones, and hence seed ger-

and Müller, 2003). mination, can be used as a very effective tool for enhanced seed

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

germination, and hence crop production. Future research could Brady, S.M., Sarkar, S.F., Bonetta, D., McCourt, P., 2003. The ABSCISIC ACID

INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved

beneﬁcially focus on how the combination of appropriate agricul-

in auxin signaling and lateral root development in Arabidopsis. Plant J. 34,

tural strategies and biological methods, such as use of soil bacteria, 67–75.

can provide a proper medium for the germination and growth of Cacciari, I., Lippi, D., Pietrosanti, T., Pietrosanti, W., 1989. Phytohormone-like sub-

stances produced by single andmixed diazotrophic cultures of Azospirillum and

seeds under a range of conditions. More details have yet to be indi-

Arthrobacter. Plant Soil. 115, 151–153.

cated related to hormonal signaling during seed germination and

Cao, S., Xu, Q., CaoY, Quian, K., An, K., ZhuY, Bineng, H., Zhao, H., Kuai, B., 2005. Loss

seed biology. For example, how it is possible to regulate seed ger- of function mutations in DET2 gene lead to an enhanced resistance to oxidative

stress in Arabidopsis. Physiol Plant. 123, 57–66.

mination at dormancy and how the speed of seed germination may

Chen, J., 2008. Heterotrimeric G-proteins in plant development. Frontiers Biosci. 13,

increase by adjusting seed behavior under different conditions.

3321–3333.

Chibani, K., Ali-Rachedi, S., Job, C., Job, D., Jullien, M., Grappin, P., 2006. Proteomic

analysis of seed dormancy in Arabidopsis. Plant Physiol. 142, 1493–1510.

Conﬂict of interest

Chiwocha, S.D., Cutler, A.J., Abrams, S.R., Ambrose, S.J., Yang, J., et al., 2005. The etr1-2

mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and

The authors declare that they do not have any conﬂict of interest. gibberellin metabolic pathways during maintenance of seed dormancy, moist-

chilling and germination. Plant J. 42, 35–48.

Choi, H.I., Park, H.J., Park, J.H., Kim, S., Im, M.Y., Seo, H.H., Kim, Y.W., Hwang, I., Kim,

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