Dormancy and germination responses of halophyte seeds to the application of ethylene

M. Ajmal Khan; Raziuddin Ansari; Bilquees Gul; Weiqiang Li

doi:10.1016/j.crvi.2009.05.002

Plant biology and pathology / Biologie et pathologie végétales

Dormancy and germination responses of halophyte seeds to the application of ethylene

Présenté par : Philippe Morat

M. Ajmal Khan ¹ ; Raziuddin Ansari ¹ ; Bilquees Gul ¹ ; Weiqiang Li ²

¹ Institute of Sustainable Halophyte Utilization, University of Karachi, Karachi 75270, Pakistan
² Plant Science Center, RIKEN, Institute of Physical and Chemical Research, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan

Comptes Rendus. Biologies, Volume 332 (2009) no. 9, pp. 806-815.

Résumé

Ethylene is invariably produced during seed germination but its role in regulating seed dormancy and germination is poorly understood. Seeds of 22 halophytic species having different life forms – salt secreting dicots, salt secreting monocots, stem succulents and leaf succulents were germinated in Petri dishes kept in a growth chamber set at 20/30 °C (night/day) temperature and a 12 hr light period. Sodium chloride and ethephon were added to the medium from the beginning of the experiment. Seed germination was recorded every other day for twenty days. Application of ethylene did not have any significant effect on releasing seeds from innate dormancy. However, it appeared to have a role in alleviation of salinity effects which varied from negative in certain species to almost complete alleviation of high salinity effects in others.

Our data indicates that ethylene appears to have little role in breaking innate seed dormancy however, in most halophyte seeds studied, application of ethylene alleviate the salinity effect to various degrees. Halophyte seeds which could germinate under saline conditions approaching twice the salinity of seawater may offer clues to understand management of seed germination under highly saline conditions.

Métadonnées

Reçu le : 2009-03-21
Accepté le : 2009-05-12
Publié le : 2009-06-26

PMID

DOI : 10.1016/j.crvi.2009.05.002

Mots clés : Dormancy, Ethephon, Germination, Halophyte seed, Salt tolerance

Affiliations des auteurs :

M. Ajmal Khan ¹ ; Raziuddin Ansari ¹ ; Bilquees Gul ¹ ; Weiqiang Li ²

¹ Institute of Sustainable Halophyte Utilization, University of Karachi, Karachi 75270, Pakistan
² Plant Science Center, RIKEN, Institute of Physical and Chemical Research, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan

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     pages = {806--815},
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M. Ajmal Khan; Raziuddin Ansari; Bilquees Gul; Weiqiang Li. Dormancy and germination responses of halophyte seeds to the application of ethylene. Comptes Rendus. Biologies, Volume 332 (2009) no. 9, pp. 806-815. doi : 10.1016/j.crvi.2009.05.002. https://comptes-rendus.academie-sciences.fr/biologies/articles/10.1016/j.crvi.2009.05.002/

Version originale du texte intégral

1 Introduction

Germination begins in dry seed with water imbibition followed by activation of biochemical systems leading into rupture of the covering layer and culminates with the emergence of radicle [1,2]. This process is inhibited by substrate salinity because of: (i) inadequate imbibition; (ii) ionic toxicity; (iii) interference with metabolism; (iv) destruction of enzymes; and (v) imbalance of growth regulators [3]. Seeds of halophytes are generally more tolerant to salinity and temperature stress during their storage in the soil and usually germinate during spring in temperate regions or after monsoon rains in sub-tropical areas when temperature and soil salinity is reduced [4]. At the time of germination, however, these seeds also become more sensitive to small perturbations in salinity, water, light and temperature regimes [3,5].

Ethylene, a known modulator of auxins, gibberellins, cytokonins, and abscisic acid during seed maturation [6,7], is released during seed germination but disagreements exist about its precise role in breaking dormancy and/or inducing germination [2,8]. It has been argued whether this gas production is a requirement for germination or it is just a consequence of reactions during germination as a major peak of ethylene evolution coincides with the completion of germination, but ethylene production is detectable very early during imbibition and before radicle emergence [6].

It is fairly well documented that ethylene removes primary dormancy [9–13], secondary dormancy [14], light induced dormancy [10], and that it reduces salinity, high temperature and osmotic stress on seed germination [15–24]. However, it has also been observed that an exogenous supply of ethylene enhances seed germination in some cases but may be ineffective or even inhibitory in other species [11].

Increasing salinization and pressure on existing fresh water resources has led to a focus on halophytes for the utilization of saline resources [25]. Seed germination, which is essential in establishing a good plant population, is drastically reduced by salinity and improving it through ethylene pretreatment under saline conditions may lead to favorable consequences. The present study was conducted on seeds of 22 halophyte species to ascertain whether the application of ethephon, an ethylene releasing compound, can alleviate the salinity effects on germination. This will provide insights into the involvement of ethylene in seed germination and may consequently lead to better management strategies for raising cash crop halophytes.

2 Materials and methods

Experiments were conducted using a number of halophytes (listed below) including salt secreting dicots (S. No. 1–5), salt secreting monocots (S. No. 6–9), stem succulents (S. No. 10–13) and leaf succulents (S. No. 14–22). These species were used to study the effect of ethylene (10 mM ethephon) on relieving innate and salinity induced seed dormancy. These seeds, which were collected from the coastal areas of Karachi, Pakistan [26], the salt marshes of Ohio County, USA and from the Great Basin Desert of Utah, USA, [27] were separated from the inflorescences and were surface sterilized using the fungicide Phygon (Hopkins Agricultural Chemical Co., Madison, Wis.). Depending on the salt tolerance of a particular species, the salinity levels used for germination are mentioned below along with the description of each species.

Germination was carried out in 50 mm × 9 mm tight-fitting plastic Petri dishes with 5 mL of test solution. Each dish was placed in a 10 cm diameter plastic Petri dish as an added precaution against loss of water by evaporation. Four replicates of 25 seeds each were used for each treatment. Seeds were considered germinated at the emergence of a radicle. Germination was carried out in a growth chamber at an alternating temperature regime of 20–30 °C where the higher temperature coincided with the 12-h light period (Sylvania cool white fluorescent lamps 25 μmol m⁻² s⁻¹, 400–750 nm) and the lower temperature coincided with the 12-h dark period. Ethephon was added at 10 mmol/L and NaCl levels were as mentioned above with the species descriptions. The controls contained the solution without salinity and ethephon treatments. Percent germination was recorded every alternate day for 20 d.

Germination data were arcsine transformed before statistical analysis to ensure homogeneity of variance. Data were analyzed using the Student's t-test ( $P < 0.05$ ) [28].

3 Results

Germination was highly variable even in the absence of salinity, ranging from poor (e.g. about 30% in C. cretica and S. ioclados species) to almost 100% in certain other species, i.e. C. lanata, K. scoparia, A. occidentalis, S. vermiculatus, L. stocksii, A. lagopoides, U. setulosa, etc. (Figs. 1 to 5). Differences were also observed between species of the same genus. For instance, S. imbricata (90% germination) was better than S. iberica (59%); S. moquinii (100%) was better than S. fruticosa (69%), and A. rosea (89%) and A. prostrata (80%) were better than A. stocksii (42%).

Fig. 1
Effect of ethephon on the final germination (mean ± SE) of secreting dicot seeds treated with various concentrations of NaCl. Asterisks indicate significant differences for Student's t-tests ( ${}^{*}P < 0.05$ , ${}^{* *}P < 0.01$ , ${}^{* * *}P < 0.001$ ).

Fig. 2
Effect of ethephon on the final germination (mean ± SE) of secreting monocot seeds treated with various concentrations of NaCl. Asterisks indicate significant differences for Student's t-tests ( ${}^{*}P < 0.05$ , ${}^{* *}P < 0.01$ , ${}^{* * *}P < 0.001$ ).

Fig. 3
Effect of ethephon on the final germination (mean ± SE) of stem succulent halophyte seeds treated with various concentrations of NaCl. Asterisks indicate significant differences for Student's t-tests ( ${}^{*}P < 0.05$ , ${}^{* *}P < 0.01$ , ${}^{* * *}P < 0.001$ ).

Fig. 4
Effect of ethephon on the final germination (mean ± SE) of leaf succulent halophyte seeds treated with various concentrations of NaCl. Asterisks indicate significant differences for Student's t-tests ( ${}^{*}P < 0.05$ , ${}^{* *}P < 0.01$ , ${}^{* * *}P < 0.001$ ).

Fig. 5
Effect of ethephon on the final germination (mean ± SE) of leaf succulent halophyte seeds treated with various concentrations of NaCl. Asterisks indicate significant differences for Student's t-tests ( ${}^{*}P < 0.05$ , ${}^{* *}P < 0.01$ , ${}^{* * *}P < 0.001$ ).

Salinity reduced germination of all species tested irrespective of life form and there was a progressive decrease with increase in substrate salinity (Figs. 1 to 5). The lowest salinity used in each case brought little reduction in germination except in S. rubra, where it reduced more than 50% compared to its control (Fig. 3) whereas other species managed more than 50% germination, with some species reaching 80–100% (Figs. 1–5). A variable but more drastic effect was evident at higher salt levels. The reduction in germination was particularly prominent at the highest salinity level where less than 15% of seeds germinated in most of the species tested. Only A. prostrata, A. rosea and H. glomeratus showed somewhat better tolerance at this salinity level, exhibiting about 40% germination compared to their respective controls (Figs. 1 and 4). At the intermediate salt level most of the species performed well with more than 50% germination. At this salinity however, germination was inhibited by about 70% in U. setulosa, S. ioclados, S. utahensis, S. moquinii, C. lanata and Z. simplex and by more than 85% in L. stocksii and S. rubra, which were very badly affected (Figs. 1 to 5).

Application of ethylene failed to bring sizeable improvement in innate dormancy in most of the halophyte seeds studied except for T. maritima and Z. simplex (Figs. 2, 4). Ethylene in the growth medium was, however, generally responsible for alleviating salinity induced reduction in germination except in S. imbricata and H. glomeratus, where germination was inhibited substantially even in the presence of ethylene with or without salinity (Figs. 4 and 5). The ethylene effect became more prominent with increasing salinity, improving germination gradually at the lowest and intermediate salt levels, and was highly visible at the highest salinity in most cases (Figs. 4 and 5).

4 Discussion

Success of any plant population is dependent on the ability of its seeds to cope with environmental conditions and have enough individuals each season reaching maturity to ensure the continuity of the lineage. Seeds of halophytes as a group are no different from other plant groups except that they have to endure high soil salinity and high temperature stress during storage in the soil. Seeds of those halophytes which could survive these extremes without losing viability would be able to maintain their population [5].

Seed germination of halophytes reported here can be grouped under three categories based on salt tolerance under saline conditions. Group one contains species whose seeds can germinate in about 300 mM NaCl, including A. prostrata, A. stocksii, T. maritima and Z. simplex. A second group consisting of species with seeds germinating in salinity about 600 mM NaCl included L. stocksii, A. lagopoides, S. ioclados, S. fruticosa and U. setulosa. A third group with species where seeds could germinate in up to 1000 mM NaCl included A occidentalis, A. macrostachyum, A. rosea, C. lanata, C. cretica, H. glomeratus, K. scoparia, S. rubra, S. utahensis, S. iberica, S. imbricata, S. vermiculatus and S. moquinii. Seeds of most of the halophytic species survive high salinity and temperature stress while in the seed bank and germinate readily when temperature and salinity stress are removed [5]. This proved true in the present study with the exception of S. vermiculatus, H. glomeratus and S. iberica (Fig. 4). The results presented also support previous reports that species are less tolerant at seed germination than at subsequent growth stage.

For the sake of convenience and ease of presentation, the effect on germination (with the control set at 100%) is tabulated showing responses at the lowest, intermediate and highest salinity levels which are represented as S1, S2 and S3 irrespective of the salt concentration in each case (Table 1). Here, S1 can vary from 25 mM NaCl in the case of Z. simplex to 300 mM in K. scoparia, and H. glomeratus etc. Similarly S2 ranges from 75 to 600 mM and S3 from 125 to 900 mM. The salt sensitivity at germination is evident from here, as S3 brought the overall germination down to 13% of control (Table 1, salinity means). Only H. glomeratus and Atriplex species exhibited some resistance and managed to germinate around 40% of the seeds at the highest salinity level. Comparison between categories of halophytes on the basis of life forms showed salt secreting dicots having the best germination (66%) followed by leaf succulents (61%), salt secreting monocots (57%) and stem succulents (51%) (Table 1, species means).

Species	Life form	Salinity	Species mean
0	S1	S2	S3
Cressa cretica	SSD	100	89	88	7	64
Atriplex prostrata	SSD	100	100	68	40	77
Atriplex stocksii	SSD	100	100	86	5	73
Atriplex rosea	SSD	100	83	47	35	66
Limonium stocksii	SSD	100	75	12	2	48
Mean		100	89	60	18	66
Triglochin maritima	SSM	100	100	65	0	66
Aeluropus lagopoides	SSM	100	94	59	6	65
Urochondra setulosa	SSM	100	70	24	3	49
Sporobolous ioclados	SSM	100	50	25	7	46
Mean		100	78	43	4	57
Ceratoides lanata	LS	100	59	26	13	50
Kochia scoparia	LS	100	90	85	29	76
Halogeton glomeratus	LS	100	86	42	37	66
Salsola imbricata	LS	100	83	53	21	64
Salsola iberica	LS	100	69	66	15	63
Sarcobatus vermiculatus	LS	100	78	42	10	58
Suaeda moquinii	LS	100	81	30	17	57
Suaeda fruticosa	LS	100	100	77	10	72
Zygophyllum simplex	LS	100	60	30	0	48
Mean		100	78	50	17	61
Allenrolfea occidentalis	SS	100	80	51	0	58
Arthrocnemum macrostachyum	SS	100	86	61	14	65
Salicornia rubra	SS	100	33	7	0	35
Salicornia utahensis	SS	100	50	34	4	47
Mean		100	62	38	4	51
Composite mean		100	78	49	13

Halophyte seeds germinate better under non-saline conditions, and the percent of seeds that germinate decreases with an increase in salinity. However, halophyte seeds may germinate at salinity concentrations much higher than the tolerance range of glycophytes [5]. Higher salinity in the medium causes osmotic and ionic effects on the species. It appears that faced with salinity, seeds of halophytes may maintain a high water potential to attain an appropriate level of hydration and protect the embryo from the deleterious effects of salt ions. Germination inhibition at higher salinity in halophytes could be due to failure of attaining minimum hydration required for germination or to protect enzymes from higher salinity, or may be due to inadequacy of seeds to manage oxidative stress created due to high water and/or ionic effect [29]. However, another important cause of germination inhibition may be the imbalance created in plant growth regulators in seeds during imbibition or later stages of activation of metabolic machinery. Seeds are known to produce inhibitors (phenolic inhibitors: [30]), particularly abscisic acid (ABA) [31]. Those seeds which failed to germinate under saline conditions due to the production of high levels of inhibitors and/or ABA could be induced to germinate with the application of growth promoters like gibberellins, ethylene and Brassinosteroids [6]. However, if the germination inhibition is caused by low availability of water or via interference with metabolism, perhaps the application of compatible solutes like proline and betaine could help by protecting enzymes from water and ionic stress [5]. Where seed germination under saline conditions is inhibited by inadequate management of oxidative stress, application of ascorbic acid may alleviate salinity effects [29].

A surge in ethylene production concomitant with, or shortly preceding, radicle emergence has been observed in a number of species [8,32–37]. The role of ethylene in the removal of dormancy and initiation of germination is debated [12]. Indeed, the very close temporal association between ethylene evolution and germination suggests a physiological link, but makes it difficult to establish the cause–effect sequence without the use of inhibitors of ethylene synthesis and perception [34,37]. Gianinetti et al. [8] showed that ethylene is not required for dormancy maintenance or release, nor is it necessary to initiate germination. Corresponding results were reported by Adkins and Ross [38] for intact oat caryopses, by Kepczynski and Karssen [18] for Amaranthus caudatus, by Machabee and Saini [32] for Chenopodium album, and by Petruzzelli et al. [33] for pea seeds. It appears that there is no general requirement for ethylene produced in the intact seeds to initiate dormancy breakage or germination [8,37].

The germination obtained in ethylene treated seeds when calculated as a percent of respective controls and presented in Table 1 above (i.e. representing salinity levels as S1, S2, S3 irrespective of salt concentration in each case) elaborated the observed beneficial effect of ethylene treatment on germination inhibited by salinity (Table 2, salinity means). It is evident from this table that ethylene treatment enhanced the germination three fold under S3 conditions compared to the control (302 against 103) and showed substantial improvement at S2 (182 against 103 in control). This increase was, however, nominal (124 against 103 in control) at S1 conditions. Comparison between categories of halophytes on the basis of life forms further substantiated the above findings. It was observed that promotion due to ethylene in salinity-inhibited germination was the highest in stem succulents (200, Table 2) having the lowest normal germination (51%, Table 1). A similar alleviating effect, but in decreasing order and magnitude, was observed in salt secreting monocots (178, Table 2 against 57% germination, Table 1), leaf succulents (165, Table 2 against 61% germination, Table 1) and salt-secreting dicots (158, Table 2 against 66% germination, Table 1). Seed germination was inhibited more when ethylene was included with salinity in the case of H. glomeratus and S. imbricata.

Species	Life form	Salinity	Species mean
0	S1	S2	S3
Cressa cretica	SSD	86	92	105	180	116
Atriplex prostrata	SSD	94	90	87	131	100
Atriplex stocksii	SSD	126	108	108	180	130
Atriplex rosea	SSD	93	107	157	174	132
Limonium stocksii	SSD	100	133	350	600	296
Mean		100	106	161	253	156
Triglochin maritima	SSM	145	100	127	–	124
Aeluropis lagopoides	SSM	100	106	169	200	144
Urochondra setulosa	SSM	102	136	118	133	122
Sporobolous ioclados	SSM	125	257	400	500	321
Mean		118	150	204	278	178
Ceratoides lanata	LS	108	181	362	683	334
Kochia scoparia	LS	104	109	119	285	154
Halogeton glomeratus	LS	61	49	33	21	41
Salsola imbricata	LS	60	69	60	63	63
Salsola iberica	LS	110	100	177	322	177
Sarcobatus vermiculatus	LS	100	73	136	200	127
Suaeda moquinii	LS	100	116	163	288	167
Suaeda fruticosa	LS	97	84	105	271	139
Zygophyllum simplex	LS	155	233	282	–	223
Mean		99	113	160	299	168
Allenrolfea occidentalis	SS	100	125	186	0	137
Arthrocnemum macrostachyum	SS	76	85	86	350	149
Salicornia rubra	SS	109	182	400	–	230
Salicornia utahensis	SS	106	184	242	600	283
Mean		98	144	228	475	200
Composite mean		103	124	182	302	–

Ethylene is reported to alleviate salinity effects on seed germination of some species but not in others. Ethylene is naturally produced during the last step of germination helping the radicle to grow faster and complete germination, or, perhaps in some species, facilitating rupture of the seed coat. Seed germination requires higher turgor in the protruding radical to pierce through the barrier however, seeds of halophytes while germinating under high saline conditions will suffer due to the loss of turgor as well as higher ABA production. Application of ethylene may restore turgor and counter the effects of ABA produced due to high salinity.

If the germination is prevented by other than physiological reasons then ethylene may not have any role, or a higher concentration of growth promoting substance might synergistically inhibit germination in the presence of ethylene. The phytohormone ethylene promoted the germination of non-dormant and dormant seeds of several species [9,11]. Ethylene is also known to alleviate thermodormancy and salt enforced dormancy [4,20]. Ethylene and ABA are reported to modulate the physiological effects caused by salinity [39]. Ethylene production during germination is reported to increase under saline conditions in crop species [40–42]. An increase in ACC level and a decrease in ACC conversion to ethylene is also reported suggesting a reduction in ACC oxidase activity.

Recent studies revealed a close connection between ethylene and ABA signaling pathways during seed germination and plant root growth [42–45]. Ethylene negatively regulates ABA action during seed germination. Ruggiero et al. [46] also showed that impaired ABA biosynthesis resulted in higher ethylene accumulation, and reduced ABA accumulation during osmotic stress may cause increased sensitivity to ethylene in the loss-of-function mutation of NCED3 [46]. Therefore, the communication between ABA and ethylene hormone signaling may direct developmental decisions under adverse environmental conditions in Arabidopsis [47,48]. Lin et al. [49] showed that ABA2-overexpressing transgenic plants with elevated ABA levels exhibited seed germination delays and greater tolerance to salinity than wild type when grown on agar plates and/or in soil. However, the germination delay was abolished in transgenic plants showing ABA levels over 2-fold higher than that of wild type grown on 250 mM NaCl. The data suggest that there are distinct mechanisms underlying ABA-mediated inhibition of seed germination under diverse stress. The mechanisms causing an antagonistic effect on ABA inhibition of seed germination remain to be illustrated. One of the possibilities is the induction of ethylene production that is also stress inducible and has an antagonistic effect on ABA action [50]. Alternatively, we still cannot exclude the possible effect of osmotic and ion toxicity, which might reduce or override ABA inhibition of seed germination at high NaCl conditions.

5 Conclusion

Literature available so far on the subject indicates the paucity of information on the mechanism of halophyte seed germination under saline conditions. Halophyte seeds which could germinate under saline conditions approaching twice the salinity of seawater may offer clues to understand management of seed germination under such conditions and may lead to more efficient cultivation practices. Ethylene, ABA and GA are believed to operate in a cascade during seed germination. Therefore, it is important that the expression of these compounds controlling halophyte seed germination gains a better understanding. This is true not only for these growth regulators but other factors such as brassinosteroids and osmotic/oxidative stress.

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