Concepts of dormancy regulation in vegetative plant propagules: A review

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C O N C E P T S OF D O R M A N C Y R E G U L A T I O N IN V E G E T A T I V E P L A N T PROPAGULES: A R E V I E W N. K. G H R U N G O 0 l)epartment of Botany, North-Eastern Hill University, Shillong 793 0t4, India

, Received 13 ,Janua U' 1992: accepted in revi,~edji~rm 3 ,]i~(~, 1992 ) CIIRUNGOO N. K. [email protected] o/" dormancy, regulation il, +,rgelalive planl pr@agules." a review. ENVIRONMENTAl.ANI) EXPFRIMENTAI,BOTANY32, 309 318. I!)92. The mechanisms controlling the onset of renewed bud growth and development of floral primordia in vegetative plant propagules defy easy explanations. The basic developmental tunctions including the onset and release of bud dormancy appcar to be under the control of several biochemical/physiological signals, all of which must bc permissive to achieve normal growth. The multifactnrial modcl of control, which implicates changes in growth hormones, respiratory substrates, nucleoproteins and genc activation as the effective signals in the regulation of bud growth and flowering, best accounts tbr the complexity of Ille process. Each individual ti*ctor in the regulatory complex appears to control specific cvents of morphogencsis, the whole process being triggered only when a harmonious integration of the required factors is achieved. An understanding of the molecular 1)iolog} of tile process is, however, still a lield of ignorance, and investigations in the area with l)lant e~rnwth rt'gtdatnr iP(;R~ and dcvelo nncntal mutants as tools would yield vital clues in tmdcrstanding the pro('css.

INTRODUCTION

IN plant species r e p r o d u c i n g vegetatively, vlz. potato, gladiolus, iris, crocus, etc., the p r o p a g u l e m a y be a modified stem, root or leat~ In a d d i t i o n to achieving multiplication of the species, vegetative propagules m a y also ensure survival of the species d u r i n g u n t a v o u r a b l e e n v i r o n m e n t a l conditions through various a d a p t i v e strategies. As in seeds, manila-station of the adaptix e strategy in vegetative propagules is suspended growth in the buds and low metabolic activity in the tissues. Such an adaptiw" strategy, i.e. " d o r m a n c y " , has been described by AM~:N:~ as an endogenously controlled t)ut e n v i r o n m e n t a l l y imposed temp o r a r y suspension of growth. HOBSON 5" regards d o r m a n c y as a ['ull or p a r t i a l inhibition of the d e v e l o p m e m a l sequence which can be reversed by well-defined physiological treatments. REES ' >' considers the a d a p t i v e strategy as growth inhi-

bition caused by an external factor o p e r a t i n g through an internal mechanism or an innate mechanism only. Considerable work has been done on the physiology of the a d a p t i v e mechanisms developed by plants p e r e n n a t i n g and p r o p a g a t i n g through vegetative propagules. T h e present p a p e r is an a t t e m p t to review the current status of our knowledge r e g a r d i n g the cause and consequence relationships tbr d o r m a n c y regulation in \'egetative i)lant propagules.

ROLE OF HORMONES

Even though i! has been sugoested that the periodicity of various phases of growth is maintained by a balance in the levels of endogenous growth regulators, :<,~+,m.m+,'., clear evidence ot a cause and consequence relationship is yet to emerge. 309

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Some of the earliest work indicating that inhibitors were involved in the regulation of dormancy was conducted by HEMBEROand his co-workers 47' who correlated dormancy of potato tubers with the presence ofa fl-inhibitor complex in the tuber tissues. Hemberg was, however, unable to inhibit the growth of potato buds by these substances, which were extracted from the potato. The flinhibitor complex theory fbr the control of dormancy was contested by BURTON~1~ tbr he could not obtain any correlation between dormancy and the level of inhibitor in the storage tissues of" potato. Burton emphasized that if an inhibiting substance were to be postulated as controlling dormancy, then it must be shown to inhibit the growth of potato sprouts. RAPPAPORT and WOLF 7~;~ reviewed the control of dormancy in potato buds and concluded that the substances that appeared to be the most involved were gibberellins and abscisic acid. The correlation of changes in the chemically identified and estimated gibberellins and abscisic acid in potato buds with dormancy could, however, not be established. Based on their observations on the quantitative changes in the levels of abscisic acid and gibberellin-like activity during wtrious phases of development in corms of saffron crocus, Koul. and FAROOQ::'4 and FAROOOand KOULc;4 suggested that specific aspects of growth and development in the plant are controlled by the ratio of endogenous growth promoters to inhibitors at a given time. Although abscisic acid (ABA) was demonstrated to be the principal inhibitory component of the fl-inhibitor complex, c6:~ KAFELI and KADYROV:'" have suggested that the complex may include gallic acid, p-coumaric acid, cafl~ic acid and kempferol. Subsequently, ABA has been reported to be the main dormancy-inducing/ t:actor in gladiolus c~ and lwacinth. ~'~4 The role of growth promoters in the regulation of dormancy Plas also received considerable attention. ~17'45A~'7"4'!~7Increase in the level of endogenous gibberellins tbllowing release fi~om dormancy under the influence of treatments or during the emergence from dormancy under natural conditiuns has been demonstrated in tubers of potato, ~''45"~*> bulbs of iris, ~a:~ tulip, :7'8':~:~'~1 hyacinth, a4: garlic cloves `<-'' and corms ofsafl}'on crocus. ':~4 In addition to observing an increase in the levels of endogenous gibberellins and cytokinins

during the process of sprouting in potato, OBHILDALOVA el a[. ~7~' also demonstrated a movement ofgibberellin-like substances from base to apex in sprouting tubers. It was suggested that besides the changes in the level of endogenous GA, movement of'the hormone within the tissues of the propagule was also important in the regulation of dormancy. Increases in the levels of growth promoters near the end of dormancy in vegetative propagules suggest their involvement in dormancy regulation. Such a role of auxins, gibbere.llins and cytokinins in sprouting of potato tubers has been confirmed by reports of" the promotive elt~cts of exogenously applied auxhls, ~74 gibberellins 45:'u and cytokinins ~4u'!'7 on bud growth and differentiation in the plant species. Observations on the effects of" hormone application on sprouting of bulbs and corms have, howew-x, indicated species-hormone specificity tbr the process. Thus, cytokinins have been proposed to be the main operative promoters in onion bulbs, since neither gibberellins nor auxins but only cylokinins, induced sprouting in naturally or ABA-induced dormant bulbs, j's's':'~'~''-'Similarly, [i'eesia and gladiolus corms haxe also been reported to respond to cytokinins only. '~S' In contrast bulbs of hyacinth, ~7~ tulip ~ and corms of saffron crocus !~.~1 sprout in response to exogenous application ofgibberellic acid. Such an efl>ct of growth hormones could, however, be ascribed to differential permeability of the cell membranes to the applied growth regulators. The response of a plant species to an exogenously applied growth regulator also does not necessarily establish the involvement of the endogenous growth regulator in the induction of the particular response. (hNZB U R G {:~8':~!~ demonstrated that dormancy break in gladiolus is associated with a flush of ethylene and that cytokinin treatment is effective in hastening sprouting and increasing ethylene production. In iris too, ethylene treatment has been reported to cause flower initiation in bulbs too small to bc able to flower naturally. ':~° Similarly, PENDERC.RASS el al. '7"-' demonstrated that ethylene-induced deterioration of cabbage was accompanied by large changes in the levels of auxins, gibberellins and abscisic acid, thus raising the question of a cause and efl>ct relationship. Current intbrmation on hormone metabolism within storage tissues suggests that intercon-

CONCEPTS OF DORMANCY REGULATION versions ot hormones from an inactive to an active tbrm and vice versa arc important prerequisites to reactivation of" the d o r m a n t tissues. Thus, a study ofcytokinin changes during sprouting of potato tubers indicated the importance of conjugation to the movement of cytokinins from storage tissues to the regions of meristematic activity. '~a~'~' In d o r m a n t tubers, cytokinins were distributed equally a m o n g apical, lateral and internodal tissues, whih" in sprouting propagules a higher level of free cytokinins was ol)served in the apical bud region, VAN STADENand BROWN 9a have further shown thai buds and developing sprouts do not have the capacity to synthesize cytokinins and any increase in cytokinin levels in growing shoots is only a result of transport. Although gibberellii1 metabolism in storage organs has been examined less critically, AuxG el a[. ~ and RI';ES :Ttt have reported the iiwolvement of GA interconversion from bound to free tbrms in the sprouting of hyacinth, iris, tulip and lily. In tulip, AUN(; ¢I al. =~ have shown that the amount of free gibberellins, in bulbs placed under conditions conducive to sprouting, increased by 67,o over the initial level, and this increase was correlated with a rapid decrease in the levels of bound gibberellins. T h e basic framework of hormone theory of dormancy regulation is based on presumptive interactions between endogenous growth inhibitors and promoters within the tissues of the propagule. Even though a cause and consequence relationship tor the role of hormones in d o r m a n y regulation and flowering in vegetative plant propagules is difficult to establish, because d o r m a n c y release in such propagules is a process spread over a considerable period of time, there is fairly elear evidence fin" tim inw)lvement of inhibitor/ promoter interactions in the control of such processes. The picture of hormonal control is, however, biased by some otdmir dual et|bcts which depend on species, inductive conditions and (heavily) on environmental [~tctors. The hormonal theory still needs to clarify the role of growth substances in development in the intact plant. Whether the limiting fiactor is hormone eoncenlration, transport and/or the sensitivity of the meristems to the levels of endogenous hormones within a plant needs dmailed investigation.

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CARBOHYDRATE METABOLISM

Experimental evidence supporting the roh" of endogenous growth hormones in the regulation of d o r m a n c y leads to the assumption that the activation/sy'nthesis of new enzyme proteins, required [br mobilization of storage reserves, is an integral part of tile mode of hormone action. There is considerable evidence that some of the initial controlling events induced by hormones are changes in m e m b r a n e permeability. (~4 A slrong relationship between m e m b r a n e permeability and starch/sugar interconversion has been reported by SHEKHAR el al. ~u tbr slored potatncs. Subterranean vegetative propagules of plants contain large quantities of reserve polysaccharides. Depending upon the plant species, the principal polymeric carbohydrate componenl may lie starch, inulin, polyli'uctosans or even sucrose and monosaccharides such as glucose and fi'uctose. '~ Investigations on d o r m a n c y regulation in several bulbous plants, e.g. tulip, :~ hyacinth, ~': iris, ~:~.lle gladiolus~t~ and satlion (focus, '_,2,'_ llranes, suggesting that the onset of renewed growth in the buds may be influenced by changes in tile organization o[" cell meml)ranes. I,ike hot-

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mones, a cause and consequence relationship tbr carbohydrate degradation and onset of renewed bud growth has been difficult to establish. TSVKAMOTOand UENO(~ observed that temperature treatment, which caused early breakage of the rest period in gladiolus corms, always resulted in an increase in the tissue concentration of soluble sugars. However, this correlation could not provide convincing evidence of a cause and consequence relationship, fbr dormant corms of" some varieties failed to sprout despite an increase in the tissue level of soluble sugars. Obserwttions that hydrolysis of starch in bulbs of wedgwood iris preceded any morphological manifestation of growth in the buds led RODRmUES PEREIRA'~v-': and others 42'4:
sprout development in potato tubers depends completely on the import of basic materials, especially sucrose, required to produce carbon skeletons for amino acids, into the buds. It has thrther been suggested that growth could be limited by the rate of supply of one or more metabolites from the storage tissues to the developing sprouts. Such a pattern of change has also been accounted tbr in terms of increased respiratory activity in the developing buds. Correlations between respiratory activity and specific stages of bud development are, however, difficult to interpret in simple terms. Treatments which moditV the pattern of development may not modify respiratory activity in a manner specifically related to development. 'a~'a< CI,EGG and RAPPAPORT c27 proposed that the accumulation of soluble sugars is merely a consequence of hormone action that

leads to the onset of renewed growth in the buds. HALEVY el al. (43 recognized two patterns of changes in the degradation of starch in vegetative plant propagules during their sprouting. In the bulbous species the rate of degradation of starch increases gradually with bud growth and development, but in corms and tubers, release from dormancy is preceded by increases in the activity of starch-degrading enzymes and a consequent increase in the rate of starch degradation. Observations o f CHRUNGOO and FAROOO..~2' support this postulate. Although an increase in the activity of amylase during sprouting is known to occur in potato tubers, :~e bulbs of iris 4:~' and hyacinth r°' and corms of Orchis morio, ~*< amylase and starch phosphorylase are involved in starch breakdown during sprouting in Crocus corms. '~ It thus appears that a buildup in the pool of fi'ee as well as phosphorylated sugars is essential tbr sustaining growth and development of the buds in sallY'on crocus.

PROTEINS AND NUCLEIC ACIDS

Research over the past two decades has revealed that there is an almost bewildering array of changes in meristems during the onset of renewed growth.' ~4, Many of'these changes occur in widely different species or in dift~rent inductive regimes in the same species, indicating that they are probably, in a general sense, essential tbr the onset of renewed growth in the buds. Changes that are seen in all cases investigated so far are increases in: (a) RNA synthesis, (b) mitotic and DNA synthetic activities, and (c) activity of several enzymes. Induction of flowering and subsequent growth and development of floral primordia have been correlated with qualitative as well as quantitative changes in the level of soluble proteins and nucleic acids in the tissues of the propagule.: 13,22,25,28,40,73 Some of the earliest studies on the relationship between changes in the pool of nitrogenous constituents and bud growth in potato tubers were conducted by I,EWTT57 and COTRUFO and I,EVlTTf2u' Changes in alcohol-soluble and alcoholinsoluble nitrogen fractions were reported to be largely due to changes in amides and amino acids, especially asparagine and glutamine. Sprouting of potato tubers has been suggested to

CONCEPTS OF DORMANCY REGULATION

be dependent on the synthesis of proteins in their buds; the synthesis being dependent upon mobilization of amino acids from tile storage regions to the bud tissues. BARBER and STEWARD (13) observed marked changes in the protein profile in tulip bulbs during release of bud dormancy. The protein profile has been reported to be influenced by conditions that induce flowering, before the morphological manifestation of growth in the buds. Changes in the protein complement of the growing point, preceding the tbrmation of floral organs, were presumed to be due to the tbrmation of specific mRNAs, the latter originating when specific gene sequences were expressed under the influence of the stimulus. Similar observations have been made by CHRUNGOOand FAROOO,,~'~5 tot corms of saffi'on c r o c u s . CHRUNGOO and FAROOQ 2> have further suggested that enhanced synthesis of specific proteins in the propagule is an essential t'eamre of the termination of its rest period. The work of SNYDER and DESBOROUGH 9tl o n changes in the clectrophoretic profile of soluble proteins, and of KAHI, el al. ~-'3' on non-histone chromosomal (NHC) proteins, during development of potato tubers, suggested that certain proteins are specific tbr the developmental stage o[ an organ. Specific changes in N H C proteins determine changes in DNA-dependent RNApolymerase activity, which then affects protein synthesis. It has been argued that since N H C proteins can reverse histone-infiibited DNAdependent RNA synthesis in vilro, they might be interacting with DNA in vivo, modif)ing the transcriptional pattern in a way that is specific tbr certain stages of develol)InenI. ~'VECHSELBERGER el al. >° fi)llowed changes in transcriptional activity in potato tubers during their development and tbund that RNA-polymerase activity and template accessibility increased during sprouting, the enzyme activity and template accessibilit} being influenced by conditions that alti~cted flowering. Even though CL1,:(;6 and RApPAPORT '77 could not obtain any evidence of activated protein synthesis in excised potato plugs treated with GA, it was concluded that "despite tMlure to show any difli'rences with respect to early induction ofprolein synthesis in GA-trcated buds, it would not be proper to assume that none ()c('llrr('(t". I n (,'tO(ll.~ (()rills, hov~'e\er, t h e pro-

313

motive influence of GA3 on sprouting has been proposed to be mediated, at least in part, through enhanced accumulation of amino acids ill the corm tissues and their utilization in the synthesis of soluble proteins in the buds] TM The effect of some natural growth regulators, viz. GA, ABA and caflkic acid on RNA synthesis in potato tuber meristems was studied by LADYZHENSKAYA el a/. ':5'~'h was reported that GA~, which stimulated tuber sprouting, also stimulated the synthesis of high molecular weight forms of RNA characteristic of active meristems, whereas ABA and caftiqc acid inhibited the same, suggesting the involvement of GA:~-mediated stimulation of transcription-translation processes in the promotion of growth in potato tuber buds. According tO (~OI,1)BERG, 40, 40'!i, of the mRNAs in reproductive structures are organ specific as compared to 20~!o in the case of vegetative structures. GAI,STONand KAuR-SAWHNEY, '37 BAGNI el al.' m,,_,: a n d I:IALA el al. ':c' suggested that polyamines may be acting as secondary messengers in the stinmlation and regulation of nucleic acid and protein synthesis during tile release of bud dormancy. BAONI and SERAFINI-]?RACASSIN1:11; showed a close c o l relation between levels of ABA aud storage nitrogenous compounds during dormancy and their release in tubers of ttelianlhus luberosu.~. l)ccrcases in the h'vel ofABA, arginine and glutamine during the end of dormancy were lbund to be associated with a corresponding increase in the levels ofputriscine, spermidine and spermine. It was also demonstrated that ribosomes in dormant tuber tissues were incapable of supporting protein synthesis unless aliphatic polyamines were made available to the system. However, IAAactivated tissues showed no such requirement. Changes in the spermidine : putriscine ratio in the storage tissues have been correlated with floral initiation in bulbs o f l r i s hollandica/-' The hypothesis that polyamines play a role in flowering is supported by studies on a non-flowering tobacco mutant RMB7, in which these amides (polyamine and aromatic amine conjugates) are not produced under conditions that lead to floral initiation in the wild tvpe. ':~'° Certain classes of amiue conjugates have been shown to be specifically associated with difl'erent floral tissues. ,.\lthough many studies have demoustrated correlations between changes in polyamine metal)-

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olism and development in plants, where multiple stimuli and transduction pathways interact in a network fashion, causality has been difficult to establish. A direct test of this hypothesis would require knowledge of the molecular genetics of polyamine metabolism. MARTIN-TANGUY et al. ':<' have exploited a natural transformation system in which genes controlling development are transferred from a bacterial plasmid to the plant genome wherein their expression has been studied. Such a methodology could provide molecular tools for perturbing developmental events that are more accessible than those buried in the plant genome. The mechanisms of bud d o r m a n c y and control of flower initiation defy easy explanations. The basic developmental functions including the onset and release of bud d o r m a n c y and initiation of floral primordia appear to be controlled by a nun> ber of mechanisms that transduce external signals into information with biochemical and developmental relevance. In retrospect, there are two prominent views on the subject. One view implicates hormones as the effectors of developmental processes in the buds borne on vegetative propagulesJ 44'8a'94~ The hormonal model, however, seems to be as tenacious as the florigen concept of flowering. It advocates the inductive role of growth substances which convey the information through movement and as concentration gradients.' 15,771 The main problem, however, is the lack of comprehensive studies that relate in welldefined experimental systems, changes in proportions, levels, metabolism and fluxes of these substances as well as the sensitivity of the meristems to these regulators with successive steps of the flowering process. Further studies in the field of genetically modifying hormone levels in plants and the effect of such changes in control of flower initiation could be quite usetul in developing an understanding of the process. P G R mutants would thus be a tool of choice in such investigations. The other view implicates a multifactorial model of control for the process. Besides implicating assimilates as the controlling factors and thus incorporating the nutrient diversion idea, =~i~ the hypothesis proposes that bud growth in vegetative propagules is regulated through transcription-translatioll processes either through the inwfivement of growth regulators present in

the tissues, 23'56'75'a9'1°1)polyamines, (~°,:~7) changes in histone chromosomal proteins/Ss) or through a combination of all of these factors. The relay model of HESLoP-HARRISON (49) or GREEN (41) implies that organs of each whorl in a meristem differentiate as a result of activation of an organspecific gene complex. The whole idea of investigation is particularly important in the understanding of physiological and biochemical aspects of reproductive biology. However, as long as the key regulatory genes are not identified, cloned and analysed, the manner and level at which such distinct molecules operate within the developmental pathway will remain obscure and controversial. Acknowledgments The author thanks the Head of the Department of Botany, for providing the necessary thcilities, and gratefully acknowledges the helpful suggestions received from Prof. S. Farooq, Department of Botany, University of Kashmir, Srinagar (India), during the preparation of the manuscript.

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CONCEPTS OF DORMANCY REGULATION

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