Yield maintenance under drought: expansive growth and hydraulics also matter in reproductive organs

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Yield maintenance under drought: expansive growth and hydraulics also matter in reproductive organs

Olivier Turc, Vincent Oury, Yves Gibon, Duyên Prodhomme, Francois Tardieu

To cite this version:

Olivier Turc, Vincent Oury, Yves Gibon, Duyên Prodhomme, Francois Tardieu. Yield maintenance under drought: expansive growth and hydraulics also matter in reproductive organs. Interdrought V, Feb 2017, Hyderabad, India. 2017. �hal-01605905�

1UMR 759 Laboratoire d’Ecophysiologie des Plantes sous Stress Environnementaux (LEPSE), INRA Montpellier, France

2UMR 1332 Biologie du Fruit et Pathologie (BFP), INRA Bordeaux, France

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Perform realistic water deficits and abortion rates in controlled platforms Four maize hybrids were grown in pots and subjected to different levels of soil water availability in greenhouse and growth chamber experiments (Phenodyn phenotyping platform). Soil water status was managed by weighing pots and adjusting water supply to the target soil water content. Three treatments were applied from tassel emergence (TE) to 7d after first silk emergence (SE), namely well watered (WW), mild deficit (WD1) and moderate deficit (WD2), with soil water potential above –0.10 MPa, around –0.25 MPa and around –0.50 MPa respectively (Fig. 1A). Their impacts on photosynthesis (Fig. 1C), transpiration (Fig. 1B) and seed set (Fig. 2) were similar to those commonly observed in drought prone fields.

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^Summary

Yield maintenance under drought in maize (Zea mays) is associated with flowering synchrony which requires the rapid extension of styles and stigma (silks) to be accessible for pollen. We show here that the control of grain set under moderate water deficits similar to those in the field results from a developmental process linked to the timing of silk growth, itself related to expansive growth and hydraulics processes, in opposition to the common view that abortion is linked to the sugar metabolism in ovaries.

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Perspectives

These results confer a pivotal role to hydraulic controls of expansive growth processes in grain yield elaboration upon changes in environmental conditions. They have large consequences in plant breeding, modelling and phenotyping.

Genotypes largely differ for the sensitivity of silk elongation rate to xylem water potential (Fig. 12), and sensitivities of silk and leaf growth were correlated (Fig. 13). This opens the way for genetic studies of the traits, genes and physiological processes controlling grain set under non-optimal climatic scenarios. These sensitivities and their genetic variability have to be included in the formalisms of crop models simulating yield in maize (e.g. APSIM model). An original method for phenotyping silk growth is currently developed by our group (companion poster IDT6-014).

Oury V, Caldeira CF, Prodhomme D, Pichon J-P, Gibon Y, Tardieu F, Turc O. 2016. Is change in ovary carbon status a cause or a consequence of maize ovary abortion in water deficit during flowering? Plant Physiology 171: 997-1008.

Oury V, Tardieu F, Turc O. 2016. Ovary apical abortion under water deficit is caused by changes in sequential development of ovaries and in silk growth rate in maize. Plant Physiology 171: 986-996.

Turc O, Bouteillé M, Fuad-Hassan A, Welcker C, Tardieu F. 2016. The growth of vegetative and reproductive structures (leaves and silks) respond similarly to hydraulic cues in maize. New Phytologist 212: 377-388.

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Carbon metabolism in ovaries was still unaffected at silk emergence

Changes in concentration and amount of sugars (Fig. 10), in activities of enzymes (Fig. 10) and in transcript levels (Fig. 11) of genes of sugar metabolism occurred 5 d after silk emergence in apical ovaries that eventually aborted, i. e. after the switch to abortion of these ovaries. Hence, we propose that, under moderate water deficits corresponding to most European drought scenarios, changes in ovary carbon metabolism during flowering time are a consequence rather than a cause of the beginning of ovary abortion.

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Silk growth is controlled by xylem water potential

Analyses of transcripts and metabolites indicate that the first molecular events induced by drought occur at first silk emergence (SE), in silks rather than in ovaries, and involve genes affecting expansive growth rather than sugar metabolism (Fig. 6). Silk elongation rate was measured using displacement transducers (Fig. 7). Time courses revealed that silk elongation rate closely followed changes in soil water status and evaporative demand, with day-night alternations similar to those in leaves (Fig. 8, Fig.

9). Day-night alternations were steeper with high than low plant transpiration rate, manipulated via evaporative demand or by covering part of leaf area (Fig. 9). Half times of changes in silk elongation rate upon changes in evaporative demand or soil water status were of 10-30 minutes (Fig. 8), similar to those in leaves, suggesting a common hydraulic control of expansive growth in both vegetative and reproductive structures.

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A switch to abortion occurs rapidly after first silk emergence.

Silk elongation rate decreased in water deficit and stopped 2-3d after first silk emergence, simultaneously for all ovary cohorts, vs 7-8d in well-watered plants.

Abortion rate in different hybrids, treatments and positions on the ear (Fig. 3) was accounted for by the superposition of the sequential emergence of silks originating from ovaries of different cohorts along the ear with the simultaneous silk growth arrest. Abortion occurred in the youngest ovaries whose silks did not emerge 2d before silk arrest (Fig. 4). This mechanism accounted for more than 90% of drought-related abortion in our experiments (Fig. 5).

Yield maintenance under drought: expansive growth and hydraulics also matter in reproductive organs

Olivier TURC

¹

, Vincent OURY

¹

, Yves GIBON

²

, Duyên PRODHOMME

²

and François TARDIEU

¹

0 200 400 600 800

WW WD1 WD2

Numberof grains or ovariesper ear A WW WD1 WD2

Number of emerged silks at silk growth arrest

Number of developed grains

800 0 200 500

0 200 400

600 B73_H MS153_H F924_H Oh43_H

R² = 0.94

0

B

WW WD2 WD1

A

WW

WD1

WD2

Abortion frequency(%)

Ovary position

0 10 20 30 40 WD2 WD1 WW 0

100 80

40 20 60

-8 -6 -4 - 2 0

Date of cohort

silk emergence relative to silk growth arrest (d)

B73_H MS153_H F924_H Oh43_H

Abortion frequency(%)

0 100

80

40 20 60

0 5 10 15 20 0 5 10 15 20 0

-1,0 -0,8 -0,6 -0,4 -0,2 0,0

Pn

Pn

leaf (MPa)

(c) (d)

(e) (f)

Control leaves covered low VPD

well watered irrigated at 18:00

irrigated at 6:00

Time of day (h)

Transpiration rate (g plant -1h -1)

Silk elongation rate (mm h 20°C-1 )

0 5 15 10 20 0 5 15 10 20

0 6 12 18 0 6 12 18 24 0

0.5 1.5

1.0 0 0.5 1.5

1.0

Time of day (h)

Silk elongation rate (mm h 20°C-1 ) ^2.0

0 1.0

2.0

0 1.0

5 6 7 8 17 18 19 20

10 min 11 min

0 0.5 1.0

1.5 0.8

0 0.4

8 9 10 11 13 14 15

24 min 17 min

IL86 silk

-1,2 -1,0 -0,8 -0,6 -0,4 -0,2 0,0

IL95 silk

-1,2 -1,0 -0,8 -0,6 -0,4 -0,2 0,0 P2

silk

-1,2 -1,0 -0,8 -0,6 -0,4 -0,2 0,0

IL129 silk

IL151 silk P1

silk CML444

silk

IL86 leaf

1 2 1 0 0 8 0 6 0 4 0 2 0 0

IL95 leaf

1 2 1 0 0 8 0 6 0 4 0 2 0 0 P2

leaf

1 2 1 0 0 8 0 6 0 4 0 2 0 0

IL129 leaf

IL151 leaf P1

leaf CML444

leaf

F252 silk

F252 leaf

1 2 1 0 0 8 0 6 0 4 0 2 0 0

Elongation rate (mm h 20°C-1 )

Ψs Soil water potential (MPa)

0 1 2 0 1 2 0 1 2 0 1 2

0 -1 0 -1 0 -1 0 -1

CML444

silk P1

silk IL129

silk IL151 silk

CML444

leaf P1

leaf IL151

leaf IL129

leaf

F252

silk P2

silk IL86

silk IL95

silk

F252

leaf P2

leaf IL95

leaf IL86

leaf

r²=0.922

Ψs required to stop leaf growth (MPa) Ψs requiredto stop silkgrowth(MPa)

-0.8 -1.1

-1.4 -1.4 -1.0 -0.6

R²=0,92

SE +5d

Cell-wall invertase activity

(nmol.min^-1.g^-1 protein)

Acid invertase activity (nmol.min^-1.g^-1

protein)

WW WD

Metabolite content (µmol.g^-1 FW)

Metabolite amount (mmol.ovary^-1) BO = basal ovaries

AO=apical ovaries

a b

b cd a

b b

c a

b b

0 c 0.5 1 1.5 2 2.5 3 3.5

d c

e e c c

d d c c

d d

B A B A

0 25

SE +5d

BO AO BO AO BO AO BO AO

c a

c c a

a

e de

bcd de

c bc c c ab bc

bc e

b

e

500

0 50

0 150

0

Starch Hexoses Sucrose WW WD

Starch Hexoses

Sucrose

Carbon metabolism

SE +5d

Starch Synthase Starch synthesis FBPase Hexokinase

Invertase SPP SPS

SuSy TPP TPS Cellulose Synthase

AGP Pectine synthesis Cellulase Pectinase Pectinesterase Expansin XET LRX Aquaporin WAK WD tolerance Lignification Expansin-like

Expansive growth

SE +5d

Expansive growth

AGP SE

Cellulase Pectinase

Pectinesterase Expansin

WAK LRX WD tolerance Lignification Pectate lyase Pectine synthesis

FBPase Hexokinase

Invertase

SPP SPS Starch Synthase Starch synthesis SuSy TPP TPS

Carbon metabolism

SE

Fig. 1

Fig. 2

Fig. 3 Fig. 4 Fig. 5 Fig. 7

Fig. 6 Fig. 9

Fig. 8

Fig. 10 Fig. 11

Fig. 12

Fig. 13