Température racinaire et accumulation à court terme de glucides chez deux hybrides de maïs au stade jeune

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Root temperature and short term accumulation of

carbohydrates in two maize hydrids at early growth

stage

J.S. Frossard, J.F. Friaud

To cite this version:

J.S. Frossard, J.F. Friaud. Root temperature and short term accumulation of carbohydrates in two

maize hydrids at early growth stage. Agronomie, EDP Sciences, 1989, 9 (10), pp.941-947.

�hal-02718333�

Plant physiology

Root

_temperature

and short

term

accumulation

of

_{carbohydrates}

in

two

maize

_hybrids

at

_early

growth

stage

J.-S.

Frossard

J.-F. Friaud

B.

Saint-Joanis

INRA, laboratoire de

_{bioclimatologie,}

domaine de _Crouelle, 63 039 Clermont-Ferrand, France (received 13 December 1988, accepted 1 October ₁₉₈₉₎

Summary —

Root and shoot

_carbohydrate

content of

_14-day

old maize

_plants

of two

_grain

_types

_(flint

and

_dent)

was

studied after 48 h

_temperature

treatment of the _{root; shoot}

_temperature

remained constant

_during

all the

_experiments.

The

_lowering

of root

_temperature

led to

_carbohydrate

accumulation in roots and shoots.

_Two-way

variance

_analysis

showed that

_only

for the accumulation of sucrose was there _any

_significant

difference between the two

_hybrids

for the

roots.

_However,

in the

shoots,

there were

_significant

differences between

genotypes

for all

carbohydrates.

The

significance

level was minimum for

starch;

at

_{10 °C,}

accumulation in dent

_type

was

_greater

than that in flint

_type.

When

testing

the

_relationship

between

_carbohydrate

accumulation;

measured and non structural

_dry

matter

_{predicted by}

our

model,

(Frossard, 1986),

there was a lack in

_precision

due to the uncertainties

surrounding

the

_input

parameters

of the

model. It was concluded that low root

_temperatures

_produce

a

_complete

overload of the root sinks and transfer

pathways.

This

_engorgement

increases starch content in

leaves,

particularly

in the dent

_genotype.

The

_study

of the effect of low root

_temperatures

on the roots must therefore deal with the whole

_plant

and not

_simply

the root.

maize -

_{genotype -}

_{seedling -}

short term -

_{carbohydrates -}

root

_{temperature -}

_modelling

Résumé —

_Température

racinaire et accumulation à court terme de

_glucides

chez deux

_hybrides

de maïs au

stade

_jeune.

L’étude de l’effet de la

_température

sur l’accumulation de

_glucides

dans les racines a été

_entreprise

pour

préciser

la nature

_biochimique

de l’accumulation de matière sèche non structurale révélée _par la modélisation

(Fros-sard,

₁₉₈₆₎

chez 2

_hybrides

de mai’s, l’un de

_{type denté,}

l’autre corné. L’abaissement de la

_température

racinaire conduit

_{rapidement (en}

48

_h)

à une accumulation de

_glucides

dans les racines et les

_parties

aériennes.

_{L analyse}

de

variance à 2 facteurs

_{(température, génotype)}

_permet

de mettre en évidence une différence

significative qui

concerne:

seulement le saccharose dans les

racines,

tous les

_glucides

dans les

_parties

aériennes. Les incertitudes d’entrée sur

les

_paramètres

du modèle ne

_permettent

_{pas de conclure} sur la nature de la matière sèche accumulée à basse

tem-pérature.

Néanmoins les résultats

_acquis

ne remettent _pas en cause les

_hypothèses

de base. On

peut

avancer que

tout se passe comme si les basses

_{températures provoquaient}

un

_engorgement

_complet

des

_puits

constitués par les

racines et des voies de

transfert;

l’effet de cet

_engorgement

se manifeste dans les feuilles

_{(augmentation}

de la teneur en

_{amidon) particulièrement}

pour le

génotype

sensible

_(type

_denté).

mai’s -

_{génotype -}

stade

_{jeune -}

court terme -

_{glucides - température}

racinaire - modélisation

INTRODUCTION

In

_previous

studies

_(Frossard,

1985,

1986),

it

was shown

that

_sensitivity

to

low

root

_temperatures

in

two

maize

_hybrids

was

_{accompanied by}

lower total

_respiration

for

the

roots of the sensitive

hybrid,

lower maintenance

_respiration

for the root

system

and

different

_{modes of energy}

use : at

10 °C the sensitive

_hybrid

accumulated more

_dry

matter than the tolerant

_{hybrid. According}

to our

model

_(Frossard,

_1986),

this accumulation is

not true

_growth.

Does it therefore result from

a

particular physiological

behaviour?

Various authors

have shown

that there

was

carbohydrate

accumulation

in

_{plants exposed}

to

low

_{temperatures,}

_e.g.

in

maize leaves and

roots

(Grobbelaar, 1963),

in

maize leaves

(Crawford

&

Huxter,

1977)

and in maize

seedlings

(Bourdu,

1984).

The results of Grobbelaar

₍₁₉₆₃₎

were obtained from

10-day-old

maize,

after 8

_days

of low

_temperature

treatment;

those of

Kleinendorst

&

Brouwer

(1970)

after

a

short

_temperature

treatment but

only

on

leaves

of 8th leaf

_stage

_plants.

No result

concerning

the short

term

effect of

root

temperature

on

_carbohydrate

accumulation

in

shoots

and roots of maize

_seedlings

_appear to

have been

_published.

_{Nevertheless,}

we can assume _{that it may} not be as different as those

cited above.

As

our

_previous

studies have shown that the accumulation of

_dry

matter in maize root

_systems

at

low

_temperature

cannot

be considered

_simply

as true

_growth,

we decided to

_study

the effect of

root

_temperature

on

_carbohydrate

accumulation

in different

_parts

of the

_plant

and the relation

between

_{carbohydrates}

and non-structural

_dry

matter as

described

_by

our model. As this

accumulation

_period

in

the

_plants

was short

(48 h)

relative to the duration of

_previous

experiments (Frossard,

1985,

1986),

we focused

mainly

on

soluble

_{carbohydrates}

and starch.

MATERIAL AND

METHODS

Plant material

As in

_previous

studies

_(Frossard,

₁₉₈₅₎

two

_single

hybrids

were used :

F7xF2,

flint

_type,

tolerant to low

spring

temperatures

in normal field cultivation

conditions, and WHxWJ, dent type,

chilling

sensitive. The

_plants

were grown on a well aerated nutrient solution as

_previously

described. The

_temperature

of

the shoots and roots was 20 °C.

During

temperature

treatement, carried out when the

plants

were 14

_days

old,

root

_temperatures

were 10, 15, 20

(controls)

and 25 °C.

Carbohydrate

assay

Carbohydrate

metabolism is not constant

_during

a

light-dark

period

(24 h) :

root

_respiration

has been

observed with a

_{daily rythm (Frossard, 1985).}

To avoid the effects of these

fluctuations,

samples

were

_always

taken at the same time : 30 min before the

_beginning

of the

_light

_phase,

48 h after the

_beginning

of the

temperature

treatment. The roots and shoots of 4

_pairs

of

_plants

from each treatment were fixed in

_liquid

nitrogen,

freeze dried and

_ground

to pass a

_125-pm

mesh. Plant material was extracted with 80 °GL ethanol and

_enzymatic

_assays

₍₃

_per

_replicate)

were

performed

to determine starch and

_simple

_sugar

content :

_glucose

with

_glucose

oxidase

_(Jourdan,

1980),

and sucrose, first with

invertase,

then with

glucose

oxidase

_(Mercier

&

_Tollier,

_1982).

The starch was autoclaved and

_hydrolysed

with

amyloglucosidase.

The

_glucose

released was

_assayed

with

_glucose

oxidase

_(Thivend,

1965 in Mercier &

Tollier,

1982). Soluble

carbohydrate

content was

determined with the anthrone method

_(Halhoul

&

Kleinberg,

1972; Mercier &

_Tollier,

_1982).

The nature _{of the sugar} was first determined with

HPLC

_(Agronomy

_{Station, INRA,}

Clermont-Ferrand-Theix).

The

_{carbohydrates}

in the eluates were

_mainly

glucose

and sucrose, with a small amount of fructose

in roots treated at 10 °C.

Statistical

_analysis

Having

checked that the statistic distributions were

Gaussian,

we tested the differences between

temperature

treatments and

_genotypes

with a

_two-way

variance

_analysis.

To

_give

a clearer

_picture

of the effect of

_temperature

on

_carbohydrate

concentration,

the results were fitted to an

_exponential

function :

y(e) carbohydrate

concentration

_{(in g/100gDW)}

at

temperature

0

_(°C);

a and b: coefficients

_{(fitted by}

non-linear

_regression)

Our

model :

a recall

From data taken from

_{growth analysis}

and

_respiration

measurements on roots at different root

temperatures

(Frossard

1985,

1986),

and

_using

the definitions of

growth respiration

and maintenance

_respiration

proposed

elsewere

(Thornley,

1970, 1977, 1982;

Mc

Cree,

1974;

Szaniawski,

1981

), we developed

a model

of energy use in roots

_{(Frossard, 1986),}

the

parameters

of which are recalled in Table I.

This model allowed us to define different situations

of _energy use for

_{growth respiration}

_(Rc,),

maintenance

_{respiration (Rm,),}

structural

_dry

matter

accumulation

_(AMs,)

and non-structural

_dry

matter

accumulation

_{(OMns,), according}

to root

_temperature.

Comparison

of

model

forecasts and

carbohydrate

contents

As the model did not

_predict

the biochemical nature of

the non-structural

_dry

matter accumulated in the roots,

we

_compared

this accumulation with that of all

carbohydrates (starch

+ sucrose +

_glucose

+

_fructose).

Let

_P(G,)

be the increase in

_carbohydrate

content

(relative

accumulation of

_{carbohydrates)}

induced

_by

the variation in

_temperature

as

_compared

with controls maintained at

20 °C,

and

_P(AMns,)

the relative accumulation of non-structural

dry

matter

_{predicted by}

the model. With :

[G]

o

carbohydrate

concentration of roots, relative to

total

_dry

matter, at

_temperature

6.

This

_expression

can also be written as:

P(G,)

e

=

(MGrg

/ M,

O

)-

(MG,

20

/

M

,

20

)

(

3

)

MG,

e

root total

_{carbohydrate weight,}

at

_{temperature 0;}

M

And :

AMnS

re

non-structural

_dry

matter accumulation of roots at

_temperature

_e, calculated from the model

_(Frossard,

1986).

According

to the

_hypothesis

of the model of _energy

use in the roots

_{(Frossard, 1986), OMns,}

_e

= 0 if

6 > 20 °C. Thus

_ðMns,2o

0.

P(AMnsr)o = amns

r

g

/

_M,

_e

₍₅₎

RESULTS AND DISCUSSION

Effect

of root

temperature

on the accumulation of

_{carbohydrates}

in the roots

Low root

_temperature

induced

_carbohydrate

accumulation in the roots

_{(Fig. 1).}

Starch content,

which was

_already

low in

controls

_{(at 20 °C),}

was not

modified

_by

the

temperature

change

but

was

different for the

two

genotypes

(Table 11).

The effect of

_temperature

on

the accumulation

of soluble

_{carbohydrates}

was

similar

in

both

hybrids.

The

_pattern

of variation of this

accumulation can be reduced to an

_exponential

function

_{(Table 111).}

In

WHxWJ,

a

_hybrid

sensitive

to low

_{temperatures,}

the accumulation was

always

lower

than that

in

F7xF2,

a tolerant

hydrid, irrespective

of the chemical nature of the

carbohydrate analysed (Fig. 1).

However,

a

_two-way

variance

_analysis

showed

that

_only

the accumulation

of

sucrose was

significantly

different

for

the two

hybrids (Table

II).

The tolerant

_hybrid

had

the

_{highest respiration}

rate at 10 °C

_{(Frossard, 1985)}

and the

_greatest

respiratory

substrate

concentration.

This result is consistent with others obtained elsewhere : on

tomato,

in the

_{range of values}

recorded,

respiratory activity

at 10 °C was almost

independent

of

_carbohydrate

content

_(Gary,

1988).

The

_hypothesis

of an accumulation of

carbohydrates,

as induced

_by

a low level of

respiration,

at

low

_temperature,

is not

tenable.

Effect of

root

_temperature

on

_carbohydrate

accumulation in shoots

A

reduction

in root

_temperature

_produced

an

(Fig. 2)

similar to that

observed

in other

species

(Gary, 1988).

The variation of this accumulation

can also be fitted to an

_exponential

function

(Table IV).

The

_two-way

variance

_{analysis (Table}

II)

showed

_{that, except}

for sucrose, there were

significant

differences between

_genotypes.

The

significance

level was minimum

for

starch;

at

10 °C,

accumulation in WHxWJ was

_greater

than

that

in F7xF2.

During

the

_period

of

_temperature

treatment,

the net assimilation rate was not modified

_by

the

lowering

of root

_temperature

_(Frossard,

_1985).

Prioul

₍₁₉₈₄₎

observed that shoot to root

transfers in maize were not very sensitive to

temperature;

hence it

is

_unlikely

that

transfer

would be

_{impaired by}

a

10 °C

_temperature.

It is

possible

therefore that the

_slowing

down of

root

_respiration

caused

_by

lowering

of

the

temperature,

which results in a decrease in the

carbohydrate

utilization,

also affects

the shoots. In other

words,

the

_{carbohydrate requirements}

of the root sinks would be

_sufficiently

affected

_by

temperature

to

_produce

an accumulation of

photosynthates

not used in

the

leaves,

as observed

_{previously (Moldau}

&

Sober,

1981)

in similar conditions.

Accumulation of

_{carbohydrates}

and mode-lization of

_energy

use in the roots

Did

_carbohydrate

accumulation

at low

temper-atures

_{rea,lly correspond}

to an accumulation of

non-structural

_dry

matter as calculated

_by

the

model? Table

V shows the values of

_parameters

calculated from

_{equations (3)}

and

_(5).

The differences

between

_P(Mns,),

calculated

from the

model,

and

_{P(G), directly}

measured,

are

not

significant

for both

_genotypes.

Thus,

the

initial

_hypothesis

can be

neither

_rejected

nor

confirmed. The values of

_P(Mns,)

_T

are very uncertain

since

_they

were the

result

of

_complex

different

_{plants (at}

_present,

it is

_impossible

to

make successive

non-destructive

measurements

of

the

increase in

_dry

_matter).

Values of

_P(G)

₁₅

are also uncertain because of the intrinsic

variability

that still remained even

_though

the

experiments

were made with F1

_hybrids

in

_highly

controlled conditions.

What, then, is the value of

our model?

- it is

probable

that the

_hypotheses

are correct.

These

_hypotheses

and

the

results

_presented

above agree with those

generally acknowledged

by

different

authors

_(as

reviewed

by

Bourdu,

1984).

However,

since

_input

numerical values are uncertain

because

of

_{methodological}

constraints and intrinsic

_variability,

there is considerable

uncertainty

about the

output

values.

CONCLUSION

When root

_temperatures

are low for a short

period,

there is a considerable accumulation of

carbohydrates

in roots and

shoots,

similar to

those observed

_by

Grobbelaar

₍₁₉₆₃₎

for

10-day-old

_plants

with 8

_days

or 20

_days

of

_temperature

treatment and

_by

Kleinendorst

&

Brouwer

₍₁₉₇₀₎

for older

_plants.

In the absence of additional

results,

it would seem that low root

_temperatures

produced

a

_complete

over load of the root sinks and transfer

_pathways.

This overload

increased starch content in

_leaves,

_particularly

in the

sensitive

genotype.

The

_study

of

the effect of low

root

_temperatures

on the roots must therefore

deal

with

the whole

_plant

and

not

_simply

the root.

Uncertainties about

the

_input

_parameters

of the

model

of available

_energy

in the roots are

such that it is

not

_possible

to come to _any

_precise

conclusion

about

the biochemical

nature of

the

accumulation of

_dry

matter observed at low

temperature.

This

_study

shows

that,

at

_{early growth}

_stage,

low

root

_temperature

_quickly

_produces

considerable

_carbohydrate

accumulation in the

whole

maize

_plant.

In

natural

conditions,

maize is often

_exposed

to low

_temperatures

at

this

_stage.

This accumulation could therefore take

_place

but it may be

only

a

_temporary

traumatism that

disappears

once

_temperature

conditions return to

normal.

It could be of interest to

_study

the same

parameters

in

_plants

_during

_temperature

treatment

_recovery.

The

_plant

_{may be able} to use

the

_{carbohydrates}

accumulated at low

temperature

to pass

throughout

a

_period

of

recuperation

without

_suffering

too much

_damage;

during

this

_period,

assimilation rate can be

greatly

affected,

particularly

in sensitive

genotypes

(Stamp, 1987).

REFERENCES

Bourdu R.

₍₁₉₈₄₎

Bases

_{physiologiques}

de I’action des

temperatures.

In:

_Physiologie

du Mais.

_Colloque

de

Royan,

15-17 mars 1983,

INRA,

389-423

Crawford R.M.M. & Huxter TJ.

₍₁₉₇₇₎

Root

_growth

and

_carbohydrate

metabolism at low temperatures. J.

Exp. Bot 28,

917-925

Frossard J.S.

₍₁₉₈₅₎

Effet de la

_temperature

des racines sur leur

_respiration

et sur la croissance des

plantules

de deux

_hybrides

de mais.

_Agronomie

5,

719-725

Frossard J.S.

₍₁₉₈₆₎

Essai de modelisation de

I’utilisation de

_1’6nergie

dans les racines.

_Application

à

1’effet de la

_temperature

racinaire chez des

_plantules

de deux

_hybrides

de maïs.

_Agronomie

6,

401-408

Gary

C.

₍₁₉₈₈₎

Relation entre

_temperature,

teneur en

glucides

et

_respiration

de la

_plante

entiere chez la

tomate en

_{phase vegetative. Agronomie}

_8,

419-424

Grobbelaar W.P.

_{(1963) Response}

of young maize

plants

to root

_{temperatures.}

Meded.

Landbouw-hogesch.

Wageningen,

63, 1-71

Halhoul M.N. &

_{Kleinberg (1972)}

Differential determination of

_glucose

and

_fructose,

and

_glucose

-and fructose -

_yelding

substances with anthrone.

Anal. Biochem. 50, 337-343

Jourdan J.

₍₁₉₈₀₎

Variations Saisonnieres de la

Morphogen6se

de la Croissance des

Syst6mes

Relations avec les Glucides et les Transferts Min6raux. These Doctorat es Sci. Université

Grenoble,

159 p + annexes

Kleinendorst A. & Brouwer R.

₍₁₉₇₀₎

The effect of

temperature

of the root medium and of the

_growing

point

of the shoot on

_growth,

water content _{and sugar}

content of maize leaves. Neth. J.

_Agric.

Sci. 18, 140-148

McCree K.J.

(1974) Equations

for the rate of dark

respiration

of white clover and

_{grain sorghum,}

as

functions of

_{dry weight, photosynthetic}

rate, and

temperature.

Crop.

Sci. 14, 509-514 4

Mercier C. & Tollier M.T

_{(1982) Separation}

et

_dosages

des

_glucides

et des

_amylases.

In : Guide

_pratique

d’analyses

dans les industries des c6r6ales

_(Godon

B.

et Loisel W.

_eds)

Lavoisier-APRIA,

273-325

Moldau H. & Sober J.

₍₁₉₈₁₎

Growth rate-reserve content

_relationship

as influenced

_by

_irradiance,

_C0

₂

concentration,

and

_temperature.

_Photosynth.

Res. 1,

217-231

Prioul J.L.

_{(1984) Transport}

et distribution des

assimilats chez le mais : m6canismes, r6le des facteurs externes. In :

_Physiologie

du Maïs.

_Colloque

de

_Royan,

15-17 mars 1983, INRA, 303-319 9

Stamp

P.

₍₁₉₈₇₎

The

_expression

of

_{photosynthetic}

traits

_during

and

_following

severe

_chilling

stress of

European

and

_tropical

maize

_genotypes.

_Physiol.

Plant 71, 73-76

Szaniawski R.K.

₍₁₉₈₁₎

Growth and maintenance

respiration

of shoot and roots in scots

_{pine seedings.}

Z.

_{Pflanzenphysiol}

101, 391-398

Thornley

J.H.M.

_{(1970) Respiration, growth}

and maintenance in

_plants.

Nature 227, 304-305

Thornley

J.H.M.

₍₁₉₇₇₎

Growth,

maintenance and

respiration :

a

_{re-interpretation.}

Ann. Bof.

41,

1197-1203

Thornley

J.H.M.

(1982) Interpretation

of

_respiration

coefficients. Ann. Bot. 49, 257-259