8/2/2019 Hormones From Roots as Signals For

1/7

r e v i e w s

H o r m o n e s fr o m ro o ts a s s ig n a ls fo rth e s h o o ts o f s t re s s e d p la n t sMichael Jackset

I n t r a c e l l u l a r s i g n a l l i n g p r o c e s s e s t h a t t r a n s l a t e h o r m o n e p e r c e p t i o n i n t o g e n e t i c ,m e t a b o l i c a n d d e v e l o p m e n t a l c h a n g e a r e t h e f o c u s o f m u c h c u r r e n t p l a n t h o r m o n er e s e a r c h . B y c h a r a c t e r iz i n g t h e s e p r o c e s s e s i t i s h o p e d t o e s t a b l i s h a n u n d e r s t a n d i n go f t h e r e g u l a t e d a n d i n t e g r a t e d b e h a v i o u r o f w h o l e p l a n t s a t t h e m o l e c u l a r l e v e l .H o w e v e r , f o r a c o m p l e t e p i c t u r e , t h e e x t r a c e l l u l a r s i g n a l li n g p r o c e s s e s t h a t c o o r d i-n a t e t h e b e h a v i o u r a n d d e v e l o p m e n t o f t h e v a r i o u s p l a n t o r g a n s m u s t a l s o b e u n c o v -e r e d . R o o t s m a y u s e h o r m o n e s , o r t h e i r p r e c u r s o r s , t o p r o v i d e s h o o t s w i t h e a r l yw a r n i n g o f d e t e r i o r a ti n g s o i l c o n d i t i o n s i n w a y s t h a t i n c r e a s e r e s i l i e n c e t o s t r es s .R e c e n t p r o g r e s s s p r i n g s fr o m i n t e g r a t e d s t u d i e s i n v o l v i n g s e n s i t i v e a n d s p e c i f i cm e t h o d s o f h o r m o n e a n a l y si s , p l a n t w a t e r r e l a t i o n s a n d t h e u s e o f g e n e t ic a l l y t r a n s-f o r m e d p l a n ts .

T e idea tha t xylem sap f lowing into the shoot systemfrom the roots carr ies not only wa ter an d m inera lnut r ients but a lso physiologica l ly ac t ive substances(hormones) tha t he lp to re la te root and shoot behaviour hasa t t rac ted physiologists for ma ny ye ars 1. The concept is bou ndup w i th the c lassic view of hormones as comp ounds producedin one place and t ransported to another , where they inf lu-ence deve lopment a s pa r t o f t he m echan i sm tha t coord ina t esthe behaviou r of di f feregt organs. Al though this i s too pre-scriptive as a definit ion for plant hormones, the idea is st i l lac t ive ly purs ued exper im enta l ly , such as in the s tudy off lower ini t ia t ion 2. Current ly , there i s m uch interest in howroots inform the shoot of de ter iora t ing soil condit ions and, inso doing, he lp the plan t a djust (accl imate) to the a l te red andmore taxing c i rcumstances.Typical reaction s to soil stres ses - such as drou ght, flood-ing, minera l nut r ien t shor tage , sa l ini ty or compact ion -inc lude slow er leaf expansion, c losure of s tomata , epinast icleaf curvature and senescence of older leaves. Trea t ingp l an t s wi th an appropr i at e ho rmone a t l ow dose s can o f t enreproduce or overcome these effec ts , and a l l the major hor-mones have been de t ec ted i n xy l em sap . Consequen tly , t he secompounds, or the i r precurso rs, have rece ived c lose a t tent ionas potential root to shoot signalling molecules. A falteringroot system could signal a s t ress condi t ion simply by adec rea se in t he supp ly o f wa te r o r m ine ra l nu t r i en t s . How-ever , ana lyses using plants wi th spl i t root systems a, orplaced in specia l ized pressure vesse ls4'5 to prevent watershortage in the shoots even when soi l i s drying or f looded,have shown tha t th is i s not necessar i ly the case . Instead,another chem ical s ignall ing mechan ism is a t work tha t g ivesear ly warnin g of de ter iora t ing soil condit ions and induceschanges above ground tha t ma y increase st ress to lerance .Convincing exper imenta l evidence to support the not ionof effec tive root to shoot s ignal l ing in s t ressed plants i s noteasi ly secured. This review summarizes the problems andident i fies possible mea ns of overcoming them. The discussionhas two main concerns: The horm one absc isic ac id (ABA) as a possible s ignal ema-na t ing f rom roo t s - ABA has been t he focus o f much recen tre sea rch wi th d rough ted p l an t s.

The way in which soi l f looding promotes epinast ic leafg rowth by m eans o f t he e thy l ene p recur so r ACC ( l -amino-cyclopropane-l-carboxylic acid) as the signalling m olecule -this i s th e mos t convincing example of root to shoot commu-nication involving a hormone.F o u r wa y s to s ig n a lThe way s i n wh ich shoo ts may sense t ha t roo t s a re unde rst ress can be placed into four ca tegories6. The two d iscussedin t h i s r ev i ew invo lve t he t r anspor t o f messenge r com-pounds d i sso lved in t he w a te r o f xy l em sap , and a re t e rmedaccording to whether they are exported to the shoots inlarger ( 'posi t ive ' messages) or smal ler ( 'negat ive ' messages)amounts as the roots become st ressed. Water i s the i r sol -ven t , and i s e i t he r d rawn up t he p l an t by in t e rna l g rad i en t sof wa ter potent ia l ge nera ted b y transpi ra t ion, or propelledmore slowly a t n ight , by radia l osmot ic gradients wi thin theroot a r i s ing f rom the ac t ive t ransp ort of ions into water-f il ledxylem e lements. Other forces may a lso move water f romroots to shoots7, a l though these rema in cont roversia l .There are two less di rec t mean s of s ignall ing, by'accumula t ion ' and 'debi t ' messages. They are t ransported inthe ph loem an d a re 'mirror imag es ' of xylem-borne posi tiveor negat ive messages. Thus, when st ress a t the roots s lowsthe export of phloem-mobi le sub stan ces f rom leaves as aresul t o f decreased sink st rength, a bui ld-up of a hormone(the accumula t ion message) can take place in the shoot . Forexample , fol ia r concent ra t ions of ABA are increased tem-pora r il y by th i s m eans w hen toma to p l an t s a re s t r e ssed bysoil f looding s . The hypothet ica l debi t m essages have not y e tbeen examined exper imenta l ly . I f they do exist , they wouldbe gene ra t ed when s t r e ssed roo ts i nc rea sed t he i r dem and fo rphloem-mobi le substance s, thus deple t ing the sho ot of sub-stances tha t inf luence i t s development . Si tua t ions wheredeb i t messages a re mos t l i ke ly t o be found include when roo tgrowth i s s t imula ted by shortage of soil n i t rogen or by infec-t ion wi th the parasi t ic weed Striga hermonthica.Ro ot to shoo t s ignal l ing: a three ph ase processThe m odel in Box 1 describes stress perception and mess-age (hormone) genera t ion in the roots (phase 1) , t ransi t of

2 2 J a n ua r y 1 9 97 , V o l , 2 , N o , 1 1 9 9 7 E l s e v i e r S c i e n c e L t d P I I $ 1 3 6 0 - 1 3 8 5 ( 9 6 ) 1 0 0 5 0 - 9

8/2/2019 Hormones From Roots as Signals For

2/7

r e v i e w s

perception in th e recip ient shoot tissues, and transdu c~on of the signal, resulting in actions b y receptive cells (e.g. causingstomatal closure) that incr ease stress tolerance (acclimation).Phase 1 Phase 2 Phase 3

Ir

Root systemStress perception

v

Signal transduction

Altered gene expressionand/or metabolismv

Increase or decrease inhormone production

Parti tioning or transportinto xylem sap '

Hormone content may become enriched or depleted as sapflows through the plants. Thus, del iveries or concentrationsin sap taken from leav es may not reflect original output fromroots below.A

After analysis of sap flowing at the rate of whole planttranspiration, the del ivery rate is estimated as:Concentra t i on Sap f l ow ra te

A

Because of di lution effects, changes in sap flow rate causedby stomatal closure can alter message concentrationindependently of del ivery rate. Thus, concentration is a po orestimate of del ivery rate.

An increase or decrease in horm one del ivery (flux) shouldbe establ ished before the existence of a positive or negativemessage can be deduced with confidence.

,. Shoot systemv

End of xylem transportsystem

Parti tioning or transportout of xylem sapv

Target cellsv

Signal perceptionv

Signal transduction

Altered gene expresstonand/or metabolismv

Developmental response

Positive or negative message?t

Xylem sap transport system to shoot

the message in the xylem sap to targets in the shoot (phase2), and message decoding in shoot t issue through a secondset of perception and intracellular tran sduction processes(phase 3). These last signals can lead, among otherresponses, to s tom atal closure, epina stic leaf curv ature , orsenescence by old leaves. The three phase system initiatesmessage formation and redirects it from a localized stresssite in the roots to remote unstressed sites in the shoot,where response characteristics to hormones are very differ-ent. Knowledge of how stresses and hormones cause sensi-tive cells to induce their effects in target cells remains rudi-mentary, but there have recen tly been exciting advances9'1.Positive and negative messages in xylem sapProblems of ana/ysisAn overriding practical difficulty arises because thexylem sap of transpiring plants is at negative hyd rostatic

(subatmospheric) pressure, making direct sampling almostimpossible. Indirect metho ds of sampling ar e needed, bu t allare problematic. Xylem sap extracted by pressurizing or cen-trifuging freshly excised shoot parts h as often been used, bu tthe m ethod runs the r isk of contaminat ing sap samples wi thsolutes from the cell wall and symplasm. Furthermore, suchsamples are often taken from tissues excised some distancefrom the roots, which could result in the solute content of thesap being changed e n route by radial transf er to or from sur-rounding tissues 11. An alternative approach has been to keepthe plant intact and apply pneumat ic p ressure to the root -the pressure is adjus ted so that the hydrostat ic pressure inthe xylem is just above atmospheric. Sap issuing from a cutin the xylem of a cotyledon close to the shoot base is thensampled 12. The solute co ncentrations and flow rate of thissap are thoug ht to be very close to those of authentic transpi-ration fluid 1~, although these assumption s have not been

January1997,Vol.2, No, 1 2 3

8/2/2019 Hormones From Roots as Signals For

3/7

~ I ~ i . ' l i i l i ] ~ l i l l i . ~ I t ] [ : ] i [ I I : i lr e v i e w s

~'E 2v

( a ) D i l u t io n o f n i t ra t ea s s a p f l o w r a t e i n c r e a s e s

I I

2 4S a p f l o w ( r a m 3 s 1)

-5E(D

z

( b ) Ef fec t on de l i v e ry o f n i t ra tea s s a p f l o w i n c r e a s e s

I I I I

1 2 3 4S a p f l o w ( m m a s - 1 )

( ( : : ) D i l u t i on o f AC Ca s s a p f l o w r a t e i n c r e a s e s ( d ) E f f e c t o n d e l i v e r y o f A C Ca s s a p f l o w i n c r e a s e s

%1 .5

0 .5

2 .0

1 ,5