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Reducing stomatal density by expression of a synthetic epidermal patterning factor increases leaf intrinsic water use efficiency and reduces plant water use in a C4 crop

Journal Article · · Journal of Experimental Botany
DOI:https://doi.org/10.1093/jxb/erae289· OSTI ID:2477470
Abstract

Enhancing crop water use efficiency (WUE) is a key target trait for climatic resilience and expanding cultivation on marginal lands. Engineering lower stomatal density to reduce stomatal conductance (gs) has improved WUE in multiple C3 crop species. However, reducing gs in C3 species often reduces photosynthetic carbon gain. A different response is expected in C4 plants because they possess specialized anatomy and biochemistry which concentrates CO2 at the site of fixation. This modifies the relationship of photosynthesis (AN) with intracellular CO2 concentration (ci), such that photosynthesis is CO2 saturated and reductions in gs are unlikely to limit AN. To test this hypothesis, genetic strategies were investigated to reduce stomatal density in the C4 crop sorghum. Constitutive expression of a synthetic epidermal patterning factor (EPF) transgenic allele in sorghum led to reduced stomatal densities, reduced gs, reduced plant water use, and avoidance of stress during a period of water deprivation. In addition, moderate reduction in stomatal density did not increase stomatal limitation to AN. However, these positive outcomes were associated with negative pleiotropic effects on reproductive development and photosynthetic capacity. Avoiding pleiotropy by targeting expression of the transgene to specific tissues could provide a pathway to improved agronomic outcomes.

Research Organization:
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
Sponsoring Organization:
USDOE; USDOE Advanced Research Projects Agency - Energy (ARPA-E); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AR0000661; SC0018420
OSTI ID:
2477470
Alternate ID(s):
OSTI ID: 2426593
OSTI ID: 2439290
Journal Information:
Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 21 Vol. 75; ISSN 0022-0957
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (78)

Natural variation of life‐history traits, water use, and drought responses in Arabidopsis journal January 2018
ggplot2 book January 2009
Sorghum (Sorghum bicolor) book September 2014
The small, versatilepPZP family ofAgrobacterium binary vectors for plant transformation journal September 1994
Rapid and reproducible Agrobacterium-mediated transformation of sorghum journal March 2006
Inheritance of Carbon Isotope Discrimination in Bread Wheat (Triticum Aestivum L.) journal March 2006
Expression of the rice CDPK-7 in sorghum: molecular and phenotypic analyses journal February 2011
Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency journal May 2013
Overexpression of maize SDD1 (ZmSDD1) improves drought resistance in Zea mays L. by reducing stomatal density journal March 2015
The Signaling Peptide EPF2 Controls Asymmetric Cell Divisions during Stomatal Development journal May 2009
Regulation of hair cell and stomatal size by a hair cell-specific peroxidase in the grass Brachypodium distachyon journal May 2023
Allometric relationships between nitrogen uptake and transpiration to untangle interactions between nitrogen supply and drought in maize and sorghum journal October 2020
The Sorghum bicolor genome and the diversification of grasses journal January 2009
Sustainable bioenergy production from marginal lands in the US Midwest journal January 2013
The NMR structure of stomagen reveals the basis of stomatal density regulation by plant peptide hormones journal September 2011
Diverging importance of drought stress for maize and winter wheat in Europe journal October 2018
Mesophyll porosity is modulated by the presence of functional stomata journal June 2019
Evidence of anthropogenic impacts on global drought frequency, duration, and intensity journal May 2021
Optimization can provide the fundamental link between leaf photosynthesis, gas exchange and water relations journal September 2020
Genetic strategies for improving crop yields journal November 2019
Rice plants overexpressing OsEPF1 show reduced stomatal density and increased root cortical aerenchyma formation journal April 2019
Molecular control of stomatal development journal January 2018
Biochemical Models of Leaf Photosynthesis book January 2000
Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive? journal January 2005
Potential yield and water-use efficiency benefits in sorghum from limited maximum transpiration rate journal January 2005
Is transpiration efficiency a viable plant trait in breeding for crop improvement? journal January 2012
Population genomic and genome-wide association studies of agroclimatic traits in sorghum journal December 2012
Variation in MPK12 affects water use efficiency in Arabidopsis and reveals a pleiotropic link between guard cell size and ABA response journal February 2014
Grasses use an alternatively wired bHLH transcription factor network to establish stomatal identity journal July 2016
Comparative expression analysis of two sugarcane polyubiquitin promoters and flanking sequences in transgenic plants journal January 2003
Transpiration, and Nitrogen Uptake and Flow in Two Maize (Zea mays L.) Inbred Lines as Affected by Nitrogen Supply journal January 2007
C4 photosynthesis and water stress journal May 2008
Improving C4 photosynthesis to increase productivity under optimal and suboptimal conditions journal July 2021
Progress and challenges in sorghum biotechnology, a multipurpose feedstock for the bioeconomy journal October 2021
Greater aperture counteracts effects of reduced stomatal density on water use efficiency: a case study on sugarcane and meta-analysis journal July 2024
Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error journal September 2003
Breeding for high water-use efficiency journal September 2004
Impairment of C4 photosynthesis by drought is exacerbated by limiting nitrogen and ameliorated by elevated [CO2] in maize journal March 2011
Deconstructing Kranz anatomy to understand C4 evolution journal May 2014
Reduced stomatal density in bread wheat leads to increased water-use efficiency journal June 2019
Epidermal Cell Density is Autoregulated via a Secretory Peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis Leaves journal May 2009
Stomatal Density is Controlled by a Mesophyll-Derived Signaling Molecule journal December 2009
Arabidopsis Reduces Growth Under Osmotic Stress by Decreasing SPEECHLESS Protein journal November 2014
Optical topometry and machine learning to rapidly phenotype stomatal patterning traits for maize QTL mapping journal July 2021
Machine learning-enabled phenotyping for GWAS and TWAS of WUE traits in 869 field-grown sorghum accessions journal July 2021
Phenotyping stomatal closure by thermal imaging for GWAS and TWAS of water use efficiency-related genes journal August 2021
Construction of a Derivative of Agrobacterium tumefaciens C58 That Does Not Mutate to Tetracycline Resistance journal January 2001
Rising atmospheric carbon dioxide concentration and the future of C 4 crops for food and fuel journal February 2009
The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule journal July 2007
Photosynthesis, Productivity, and Yield of Maize Are Not Affected by Open-Air Elevation of CO 2 Concentration in the Absence of Drought journal January 2006
Application of Optical Topometry to Analysis of the Plant Epidermis journal August 2015
Reducing Stomatal Density in Barley Improves Drought Tolerance without Impacting on Yield journal May 2017
SHORTROOT-Mediated Increase in Stomatal Density Has No Impact on Photosynthetic Efficiency journal November 2017
Dominant-Negative Receptor Uncovers Redundancy in the Arabidopsis ERECTA Leucine-Rich Repeat Receptor–Like Kinase Signaling Pathway That Regulates Organ Shape journal April 2003
The Arabidopsis GTL1 Transcription Factor Regulates Water Use Efficiency and Drought Tolerance by Modulating Stomatal Density via Transrepression of SDD1 journal December 2010
Redefining marginal land for bioenergy crop production journal August 2021
The signalling peptide EPFL9 is a positive regulator of stomatal development journal February 2010
Photosynthetic pathway and ecological adaptation explain stomatal trait diversity amongst grasses journal November 2011
Will photosynthesis of maize ( Zea mays ) in the US Corn Belt increase in future [CO 2 ] rich atmospheres? An analysis of diurnal courses of CO 2 uptake under free-air concentration enrichment (FACE) journal June 2004
Increasing water-use efficiency directly through genetic manipulation of stomatal density journal March 2015
Manipulating stomatal density enhances drought tolerance without deleterious effect on nutrient uptake journal August 2015
Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions journal July 2018
Stomatal development in the grasses: lessons from models and crops (and crop models) journal February 2020
PdEPF1 regulates water-use efficiency and drought tolerance by modulating stomatal density in poplar journal July 2015
Transpiration increases under high‐temperature stress: Potential mechanisms, trade‐offs and prospects for crop resilience in a warming world journal December 2020
The influence of stomatal morphology and distribution on photosynthetic gas exchange journal November 2019
Direct roles of SPEECHLESS in the specification of stomatal self-renewing cells journal September 2014
Plant Productivity and Environment journal October 1982
Water Use Efficiency as a Constraint and Target for Improving the Resilience and Productivity of C 3 and C 4 Crops journal April 2019
Stomatal Conductance and Photosynthesis journal June 1982
Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses journal June 2009
SCARECROW is deployed in distinct contexts during rice and maize leaf development journal March 2022
Comparison of Nitrogen Uptake, Transpiration Rate and Exudation Rate between Upland NERICAs and Japanese Cultivars journal January 2010
Least-Squares Means: The R Package lsmeans journal January 2016
Rapid Method for Estimating Leaf Area Per Plant in Maize1 journal September 1975
Bioenergy Sorghum Crop Model Predicts VPD-Limited Transpiration Traits Enhance Biomass Yield in Water-Limited Environments journal March 2017
Water-Use Efficiency: Advances and Challenges in a Changing Climate journal February 2019
Agronomic and Energetic Potential of Biomass Sorghum Genotypes journal January 2015

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