Abstract

Drought is the most important crop yield-limiting factor, and detailed knowledge of its impact on plant growth regulation is crucial. The maize (Zea mays) leaf growth zone offers unique possibilities for studying the spatiotemporal regulation of developmental processes by transcriptional analyses and methods that require more material, such as metabolite and enzyme activity measurements. By means of a kinematic analysis, we show that drought inhibits maize leaf growth by inhibiting cell division in the meristem and cell expansion in the elongation zone. Through a microarray study, we observed the down-regulation of 32 of the 54 cell cycle genes, providing a basis for the inhibited cell division. We also found evidence for an up-regulation of the photosynthetic machinery and the antioxidant and redox systems. This was confirmed by increased chlorophyll content in mature cells and increased activity of antioxidant enzymes and metabolite levels across the growth zone, respectively. We demonstrate the functional significance of the identified transcriptional reprogramming by showing that increasing the antioxidant capacity in the proliferation zone, by overexpression of the Arabidopsis (Arabidopsis thaliana) iron-superoxide dismutase gene, increases leaf growth rate by stimulating cell division. We also show that the increased photosynthetic capacity leads to enhanced photosynthesis upon rewatering, facilitating the often-observed growth compensation.

Highlights

  • Drought is the most important crop yield-limiting factor, and detailed knowledge of its impact on plant growth regulation is crucial

  • This was associated with an even stronger inhibition of leaf elongation rate (LER) by 27% and 63% in mild and severe stress conditions, respectively (Table I), which was partly offset by an increased duration of the leaf growth period

  • Kinematic analysis, based on measurements of LER, the cell length profile along the growth zone (Supplemental Fig. S2), and the length of the meristem determined by locating mitotic cells, showed that the decrease in LER is primarily due to a strongly reduced cell production in the meristem, whereas mature cell length showed only a small reduction that was not statistically significant (Table I)

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Summary

Introduction

Drought is the most important crop yield-limiting factor, and detailed knowledge of its impact on plant growth regulation is crucial. It is increasingly being used for studies into the regulation of cell division and expansion (Rymen et al, 2007) and the environmental effects on these processes (Walter et al, 2009), redox regulation (Kravchik and Bernstein, 2013), hormone homeostasis (Nelissen et al, 2012), protein expression and phosphorylation (Riccardi et al, 1998; Bonhomme et al, 2012), and the development of the C4 photosynthetic system (Li et al, 2010; Majeran et al, 2010) Several of these studies are currently impossible in the model plant Arabidopsis (Arabidopsis thaliana) due to the small size of its meristematic and elongation zones. Gene expression varies strongly between dividing, expanding, and mature cells (Beemster et al, 2005), and the impact of osmotic and salt stress on each of these processes is distinctly different (Skirycz and Inzé, 2010), urging more development-specific studies of the impact of drought

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