Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen Entry.

Mutiara K Pitaloka,Julie E Gray,Siwaret Arikit,Supatthra Narawatthana,Watchara Phetluan,Samart Wanchana,Robert A Brench,Robert S Caine,Emily L Harrison,Apichart Vanavichit,Theerayut Toojinda,Christopher Hepworth

doi:10.3389/fpls.2021.677839

Abstract

Rice (Oryza sativa) is a water-intensive crop, and like other plants uses stomata to balance CO2 uptake with water-loss. To identify agronomic traits related to rice stomatal complexes, an anatomical screen of 64 Thai and 100 global rice cultivars was undertaken. Epidermal outgrowths called papillae were identified on the stomatal subsidiary cells of all cultivars. These were also detected on eight other species of the Oryza genus but not on the stomata of any other plant species we surveyed. Our rice screen identified two cultivars that had “mega-papillae” that were so large or abundant that their stomatal pores were partially occluded; Kalubala Vee had extra-large papillae, and Dharia had approximately twice the normal number of papillae. These were most accentuated on the flag leaves, but mega-papillae were also detectable on earlier forming leaves. Energy dispersive X-Ray spectrometry revealed that silicon is the major component of stomatal papillae. We studied the potential function(s) of mega-papillae by assessing gas exchange and pathogen infection rates. Under saturating light conditions, mega-papillae bearing cultivars had reduced stomatal conductance and their stomata were slower to close and re-open, but photosynthetic assimilation was not significantly affected. Assessment of an F3 hybrid population treated with Xanthomonas oryzae pv. oryzicola indicated that subsidiary cell mega-papillae may aid in preventing bacterial leaf streak infection. Our results highlight stomatal mega-papillae as a novel rice trait that influences gas exchange, stomatal dynamics, and defense against stomatal pathogens which we propose could benefit the performance of future rice crops.

Highlights

Rice is an integral food staple that influences economic and social prosperity (Redfern et al, 2012; Pachauri et al, 2014)
We focus on the form and function of abnormally large or abundant papillae, which are located on the subsidiary cells of stomatal complexes of particular rice cultivars, which we term “mega-papillae.”
To identify morphological traits that might aid in improving rice abiotic and biotic stress responses, we examined the abaxial flag leaf surfaces of 164 rice cultivars (Supplementary Table 1) using light microscopy to inspect leaf impressions

Summary

Introduction

Rice is an integral food staple that influences economic and social prosperity (Redfern et al, 2012; Pachauri et al, 2014). It is produced in dry, tropical and temperate climates, on average requiring around 2,500 liters of water to produce 1 kg of grain (Bouman, 2009). Oryzae (Xoo), which causes bacterial blight, and Xanthomonas oryzae pv. Oryzicola (Xoc), which causes bacterial leaf streak (BLS), will impact on future yields (Niño-Liu et al, 2006). For Xoc, which enters through the same microscopic stomatal pores that govern wateruse, yield losses can already exceed 30% (Liu et al, 2014). Despite the potential losses caused by Xoc, no studies have investigated how altering stomata on rice leaves might affect Xoc infection rate

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