Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen Entry

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...

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Main Authors: Mutiara K. Pitaloka, Emily L. Harrison, Christopher Hepworth, Samart Wanchana, Theerayut Toojinda, Watchara Phetluan, Robert A. Brench, Supatthra Narawatthana, Apichart Vanavichit, Julie E. Gray, Robert S. Caine, Siwaret Arikit
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.677839/full
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spelling doaj-884733e4e5634a98a054f055c64e8d2d2021-06-04T08:04:02ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-06-011210.3389/fpls.2021.677839677839Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen EntryMutiara K. Pitaloka0Emily L. Harrison1Christopher Hepworth2Samart Wanchana3Theerayut Toojinda4Watchara Phetluan5Robert A. Brench6Supatthra Narawatthana7Apichart Vanavichit8Apichart Vanavichit9Julie E. Gray10Robert S. Caine11Siwaret Arikit12Siwaret Arikit13Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom, ThailandDepartment of Molecular Biology and Biotechnology, University of Sheffield, Sheffield, United KingdomDepartment of Animal and Plant Sciences, University of Sheffield, Sheffield, United KingdomNational Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Khlong Luang, ThailandNational Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Khlong Luang, ThailandCenter for Agricultural Biotechnology, Kasetsart University, Kamphaeng Saen Campus, Nakhon Pathom, ThailandDepartment of Molecular Biology and Biotechnology, University of Sheffield, Sheffield, United KingdomThailand Rice Science Institute, Rice Department, Ministry of Agriculture and Cooperatives (MOAC), Suphanburi, ThailandRice Science Center, Kasetsart University, Nakhon Pathom, ThailandDepartment of Agronomy, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University Kamphaeng Saen Campus, Nakhon Pathom, ThailandDepartment of Molecular Biology and Biotechnology, University of Sheffield, Sheffield, United KingdomDepartment of Molecular Biology and Biotechnology, University of Sheffield, Sheffield, United KingdomRice Science Center, Kasetsart University, Nakhon Pathom, ThailandDepartment of Agronomy, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University Kamphaeng Saen Campus, Nakhon Pathom, ThailandRice (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.https://www.frontiersin.org/articles/10.3389/fpls.2021.677839/fullstomatasubsidiary cellspapillaesilicongas-exchangebacterial pathogen
collection DOAJ
language English
format Article
sources DOAJ
author Mutiara K. Pitaloka
Emily L. Harrison
Christopher Hepworth
Samart Wanchana
Theerayut Toojinda
Watchara Phetluan
Robert A. Brench
Supatthra Narawatthana
Apichart Vanavichit
Apichart Vanavichit
Julie E. Gray
Robert S. Caine
Siwaret Arikit
Siwaret Arikit
spellingShingle Mutiara K. Pitaloka
Emily L. Harrison
Christopher Hepworth
Samart Wanchana
Theerayut Toojinda
Watchara Phetluan
Robert A. Brench
Supatthra Narawatthana
Apichart Vanavichit
Apichart Vanavichit
Julie E. Gray
Robert S. Caine
Siwaret Arikit
Siwaret Arikit
Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen Entry
Frontiers in Plant Science
stomata
subsidiary cells
papillae
silicon
gas-exchange
bacterial pathogen
author_facet Mutiara K. Pitaloka
Emily L. Harrison
Christopher Hepworth
Samart Wanchana
Theerayut Toojinda
Watchara Phetluan
Robert A. Brench
Supatthra Narawatthana
Apichart Vanavichit
Apichart Vanavichit
Julie E. Gray
Robert S. Caine
Siwaret Arikit
Siwaret Arikit
author_sort Mutiara K. Pitaloka
title Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen Entry
title_short Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen Entry
title_full Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen Entry
title_fullStr Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen Entry
title_full_unstemmed Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen Entry
title_sort rice stomatal mega-papillae restrict water loss and pathogen entry
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-06-01
description 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.
topic stomata
subsidiary cells
papillae
silicon
gas-exchange
bacterial pathogen
url https://www.frontiersin.org/articles/10.3389/fpls.2021.677839/full
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