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Why is lateral root growth so variable? A framework to analyze growth variability among lateral roots and the possible roles of auxin and carbon

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HAL Id: hal-01268803

https://hal.archives-ouvertes.fr/hal-01268803

Submitted on 3 Jun 2020

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Why is lateral root growth so variable? A framework to analyze growth variability among lateral roots and the

possible roles of auxin and carbon

Beatriz Moreno Ortega, Emilie Chandezon, Guillaume Fort, Yann Guédon, Bertrand Muller

To cite this version:

Beatriz Moreno Ortega, Emilie Chandezon, Guillaume Fort, Yann Guédon, Bertrand Muller. Why is lateral root growth so variable? A framework to analyze growth variability among lateral roots and the possible roles of auxin and carbon. 7th International Symposium on Root Development, Sep 2014, Weimar, Germany. 2014. �hal-01268803�

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Why is lateral root growth so variable?

A framework to analyze growth variability among lateral roots and the

possible roles of auxin and carbon

Beatriz Moreno-Ortega

1

, Emilie Chandezon

1

, Guillaume Fort

1

, Yann Guédon

2

and Bertrand Muller

1

1

UMR LEPSE, INRA, Montpellier, France;

2

UMR AGAP, CIRAD and Inria Virtual Plants, Montpellier, France

contact: ortegab@supagro.inra.fr

We used a rhizotron system (Neufeld 1989) to force the root system of young maize plants to grow in 2D.

Acknowledgments : X Draye for discussions, F Hochholdinger for the auxin responsive genes, P Nacry and J Rochette for the sugar responsive genes, G Rolland for sugar analysis, C Alcon for microscopy, INRA-EA and KBBE EURoot for PhD funding.

Morphological and growth traits for each individual root were extracted using

SmartRoot (Lobet 2011) and analyzed

using R software.

LR length and diameter were highly variable among roots of the same age (i.e. neighbours along the primary root). On the basis of LR lengths at day 1-3 after emergence, we identified 3 main LR growth profiles.

A second type of roots (B) showed gradually decreasing elongation rate and a progressive decrease in apical diameter.

3 Cellular and molecular fingerprints associated with LR types

Cortical cell length patterns as a function of distance to root tip were clearly different in the 3 root classes with a much longer

meristematic zone in A compared to B and

almost a disapearance of meristem in C. The first root hair was closer to the tip in C than in A, B being intermediate.

2 We have identified 3 main LR growth profiles

1 Phenotyping LR growth in maize plants

Individual root systems were scanned daily at high resolution (720 dpi) during 15 days.

• We have established a phenotyping and analysis pipeline able to extract data on single LR growth profiles and make them usable for in-depth statistical

analysis.

• In maize, LRs can be classified in 3 contrasting types with sustained elongation and diameter (A), decreasing growth and diameter (B) and rapid cessation of

elongation (C). Decelerating (B) and arrested (C) roots show reduced meristem size while arrested roots show sugar starvation.

• Excision of seminal and nodal roots massively modified sugar and probably

auxin fluxes with consequences on both the proportion and the elongation rate of sustained growing roots (A).

• Our results support the hypothesis of a role of auxin and sugars in the control of the variability of LR growth.

• Additional experiments are needed to uncouple auxin from sugar fluxes, possibly using mutants or chemicals altering auxin transport.

5 Conclusion and perspectives

Seminal and nodal root excision

was used to alter the fluxes of

sugars and auxin from the shoot to the LRs present along the primary root.

The excised root systems

exhibited a modified proportion

of LR types, with an increased

number of type A roots and a

reduced number of short C roots and a stimulated elongation rate for A roots only.

4 Auxin and sugars are involved in the variability of LRs

Excision modified the molecular signature with reduced signs of sugar starvation in C

roots and increased signs of growth stimulation in A and B roots.

A set of 7 genes including genes responsive to

sugar starvation and auxin abundance was used

to associate root types with molecular fingerprints. A principal components analysis was used to build a molecular profile of each LR type. Type A roots have an elevated expression of CYC and EXP markers and low levels of auxin and sugar

starvation genes. Type C roots have an opposite fingerprint, while B type roots have a pattern

intermediate between A and C.

Lateral root (LR) development allows the plant to explore the soil volume and capture water and minerals resources efficiently. In most

species, annual or perenials, monocots or dicots, a large intrinsic variability in LR length is present. Such variability could be an

adaptive trait enabling a greater plasticity and efficiency of the root system considering the spatial and temporal heterogeneity of soil

resources (Forde 2009; Pagès 2011).

While the molecular pathways involved in the development of primordia and young LRs (and in particular the contributions of auxin) are

well characterized (eg. Lavenus 2013), we know surprisingly little about the mechanisms and actors involved in the variability of LRs.

Because root growth rate is dependent on assimilate availability (Freixes 2002), we hypothesized that both auxin fluxes and sugar

status of individual LRs could be involved in the variability of LR fate.

We use maize plants as a model and have developped a phenotyping and computational pipeline to aquire and statistically analyse the

LR growth patterns. Moreover, we have modified carbon and auxin fluxes to the LR using excision of all roots but the primary root and

evaluated auxin and sugar status using biochemical and molecular markers.

A third type of roots (C) showed rapid cessation of elongation reaching a length < 10 mm associated with a rapid decrease in apical diameter.

A first type of roots (called A) showed maintained elongation rate and apical diameter, giving rise to very long roots.

A

Excision induced an overflow of sugars

towards the tip of A and B roots as shown by the massive (x 20) increase of glucose

concentration in the tip of these roots.

Symbol Gene name Responsive to

EXP B4 expansin cellular elongation

CYC cyclin cellular mitosis

OMB1 asparagine synthase carbon starvation

OMB4 vacuolar invertase carbon starvation

OMB5.5b sucrose synthase carbon starvation

IAA4 unknown function auxin abundance

IAA17 unknown function auxin abundance

Treatment A (%) B (%) C(%) N plants N roots

Control 16 38 46 3 509 Excision 32 36 32 3 528 0,0 5,0 10,0 15,0 20,0 25,0 0 10 20 30 G lc (µ m o l g FW -1 ) Distance to apex (mm) 0 3 6 9 12 15 18 21 24 27 30

Distance to the apex (mm)

0 10 20 30 0,0 1,0 2,0 3,0 4,0 5,0 G lc (µ m o l g FW -1 ) A B C 10 – 20 mm zone

Forde, B G et al (2009). Journal of Experimental Botany, 60(14), 3989–4002. Freixes, S et al (2002). Plant, Cell and Environment, 25(10), 1357–1366. Lavenus, J et al (2013). Trends in Plant Science, 18(8), 450–8.

Lobet, G et al (2011). Plant Physiology, 157(1), 29–39. Neufeld, H S et al (1989). Plant and Soil, 117(2), 295–298.

Pagès, L et al (2011). Plant, Cell & Environment, 34(10), 1749–60. A-Ctrl A-Exc B-Exc B-Ctrl C-Exc C-Ctrl

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