Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple

Ching M. Wai; Robert VanBuren; Jisen Zhang; Lixian Huang; Wenjing Miao; Patrick P. Edger; Won C. Yim; Henry D. Priest; Blake C. Meyers; Todd Mockler; J. Andrew C. Smith; John C. Cushman; Ray Ming

doi:10.1111/tpj.13630

Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple

Ching M. Wai, Robert VanBuren, Jisen Zhang, Lixian Huang, Wenjing Miao, Patrick P. Edger, Won C. Yim, Henry D. Priest, Blake C. Meyers, Todd Mockler, J. Andrew C. Smith, John C. Cushman, Ray Ming^*

^*Corresponding author for this work

Biochemistry and Molecular Genetics

Research output: Contribution to journal › Article › peer-review

53 Scopus citations

Abstract

The altered carbon assimilation pathway of crassulacean acid metabolism (CAM) photosynthesis results in an up to 80% higher water-use efficiency than C₃ photosynthesis in plants making it a potentially useful pathway for engineering crop plants with improved drought tolerance. Here we surveyed detailed temporal (diel time course) and spatial (across a leaf gradient) gene and microRNA (miRNA) expression patterns in the obligate CAM plant pineapple [Ananas comosus (L.) Merr.]. The high-resolution transcriptome atlas allowed us to distinguish between CAM-related and non-CAM gene copies. A differential gene co-expression network across green and white leaf diel datasets identified genes with circadian oscillation, CAM-related functions, and source-sink relations. Gene co-expression clusters containing CAM pathway genes are enriched with clock-associated cis-elements, suggesting circadian regulation of CAM. About 20% of pineapple microRNAs have diel expression patterns, with several that target key CAM-related genes. Expression and physiology data provide a model for CAM-specific carbohydrate flux and long-distance hexose transport. Together these resources provide a list of candidate genes for targeted engineering of CAM into C₃ photosynthesis crop species.

Original language	English (US)
Pages (from-to)	19-30
Number of pages	12
Journal	Plant Journal
Volume	92
Issue number	1
DOIs	https://doi.org/10.1111/tpj.13630
State	Published - Oct 2017

Funding

Gene family expansion was previously proposed as the driver of CAM pathway evolution through neofunctional-ization of newly duplicated gene copies (Silvera et al., 2010; Cai et al., 2014). Pineapple has a normal number of CAM pathway genes, carbohydrate, transporters and stomatal movement genes compared with other CAM, C3, and C4 photosynthesis species (Ming et al., 2015). Thus, CAM in pineapple has probably evolved through the regulatory neofunctionalization of pre-existing gene copies, this hypothesis is supported by enriched clock-associated cis-regulatory regions in key CAM pathway genes. This finding suggests that CAM activity could be engineered through the reprogramming of regulatory regions of pre-existing C3 genes that govern nocturnal CO2 uptake and fixation and cognate stomatal movement genes to shift stomatal opening to the night-time.

Keywords

Ananas comosus
CAM photosynthesis
circadian regulation
cis-element
stomata

ASJC Scopus subject areas

Genetics
Plant Science
Cell Biology

Access to Document

10.1111/tpj.13630

Cite this

@article{a8f3f82e0bb04f2ea17884b9f3c9ab68,

title = "Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple",

abstract = "The altered carbon assimilation pathway of crassulacean acid metabolism (CAM) photosynthesis results in an up to 80% higher water-use efficiency than C3 photosynthesis in plants making it a potentially useful pathway for engineering crop plants with improved drought tolerance. Here we surveyed detailed temporal (diel time course) and spatial (across a leaf gradient) gene and microRNA (miRNA) expression patterns in the obligate CAM plant pineapple [Ananas comosus (L.) Merr.]. The high-resolution transcriptome atlas allowed us to distinguish between CAM-related and non-CAM gene copies. A differential gene co-expression network across green and white leaf diel datasets identified genes with circadian oscillation, CAM-related functions, and source-sink relations. Gene co-expression clusters containing CAM pathway genes are enriched with clock-associated cis-elements, suggesting circadian regulation of CAM. About 20% of pineapple microRNAs have diel expression patterns, with several that target key CAM-related genes. Expression and physiology data provide a model for CAM-specific carbohydrate flux and long-distance hexose transport. Together these resources provide a list of candidate genes for targeted engineering of CAM into C3 photosynthesis crop species.",

keywords = "Ananas comosus, CAM photosynthesis, circadian regulation, cis-element, stomata",

author = "Wai, {Ching M.} and Robert VanBuren and Jisen Zhang and Lixian Huang and Wenjing Miao and Edger, {Patrick P.} and Yim, {Won C.} and Priest, {Henry D.} and Meyers, {Blake C.} and Todd Mockler and Smith, {J. Andrew C.} and Cushman, {John C.} and Ray Ming",

note = "Funding Information: Gene family expansion was previously proposed as the driver of CAM pathway evolution through neofunctional-ization of newly duplicated gene copies (Silvera et al., 2010; Cai et al., 2014). Pineapple has a normal number of CAM pathway genes, carbohydrate, transporters and stomatal movement genes compared with other CAM, C3, and C4 photosynthesis species (Ming et al., 2015). Thus, CAM in pineapple has probably evolved through the regulatory neofunctionalization of pre-existing gene copies, this hypothesis is supported by enriched clock-associated cis-regulatory regions in key CAM pathway genes. This finding suggests that CAM activity could be engineered through the reprogramming of regulatory regions of pre-existing C3 genes that govern nocturnal CO2 uptake and fixation and cognate stomatal movement genes to shift stomatal opening to the night-time. Publisher Copyright: {\textcopyright} 2017 The Authors The Plant Journal {\textcopyright} 2017 John Wiley & Sons Ltd",

year = "2017",

month = oct,

doi = "10.1111/tpj.13630",

language = "English (US)",

volume = "92",

pages = "19--30",

journal = "Plant Journal",

issn = "0960-7412",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "1",

}

TY - JOUR

T1 - Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple

AU - Wai, Ching M.

AU - VanBuren, Robert

AU - Zhang, Jisen

AU - Huang, Lixian

AU - Miao, Wenjing

AU - Edger, Patrick P.

AU - Yim, Won C.

AU - Priest, Henry D.

AU - Meyers, Blake C.

AU - Mockler, Todd

AU - Smith, J. Andrew C.

AU - Cushman, John C.

AU - Ming, Ray

N1 - Funding Information: Gene family expansion was previously proposed as the driver of CAM pathway evolution through neofunctional-ization of newly duplicated gene copies (Silvera et al., 2010; Cai et al., 2014). Pineapple has a normal number of CAM pathway genes, carbohydrate, transporters and stomatal movement genes compared with other CAM, C3, and C4 photosynthesis species (Ming et al., 2015). Thus, CAM in pineapple has probably evolved through the regulatory neofunctionalization of pre-existing gene copies, this hypothesis is supported by enriched clock-associated cis-regulatory regions in key CAM pathway genes. This finding suggests that CAM activity could be engineered through the reprogramming of regulatory regions of pre-existing C3 genes that govern nocturnal CO2 uptake and fixation and cognate stomatal movement genes to shift stomatal opening to the night-time. Publisher Copyright: © 2017 The Authors The Plant Journal © 2017 John Wiley & Sons Ltd

PY - 2017/10

Y1 - 2017/10

N2 - The altered carbon assimilation pathway of crassulacean acid metabolism (CAM) photosynthesis results in an up to 80% higher water-use efficiency than C3 photosynthesis in plants making it a potentially useful pathway for engineering crop plants with improved drought tolerance. Here we surveyed detailed temporal (diel time course) and spatial (across a leaf gradient) gene and microRNA (miRNA) expression patterns in the obligate CAM plant pineapple [Ananas comosus (L.) Merr.]. The high-resolution transcriptome atlas allowed us to distinguish between CAM-related and non-CAM gene copies. A differential gene co-expression network across green and white leaf diel datasets identified genes with circadian oscillation, CAM-related functions, and source-sink relations. Gene co-expression clusters containing CAM pathway genes are enriched with clock-associated cis-elements, suggesting circadian regulation of CAM. About 20% of pineapple microRNAs have diel expression patterns, with several that target key CAM-related genes. Expression and physiology data provide a model for CAM-specific carbohydrate flux and long-distance hexose transport. Together these resources provide a list of candidate genes for targeted engineering of CAM into C3 photosynthesis crop species.

AB - The altered carbon assimilation pathway of crassulacean acid metabolism (CAM) photosynthesis results in an up to 80% higher water-use efficiency than C3 photosynthesis in plants making it a potentially useful pathway for engineering crop plants with improved drought tolerance. Here we surveyed detailed temporal (diel time course) and spatial (across a leaf gradient) gene and microRNA (miRNA) expression patterns in the obligate CAM plant pineapple [Ananas comosus (L.) Merr.]. The high-resolution transcriptome atlas allowed us to distinguish between CAM-related and non-CAM gene copies. A differential gene co-expression network across green and white leaf diel datasets identified genes with circadian oscillation, CAM-related functions, and source-sink relations. Gene co-expression clusters containing CAM pathway genes are enriched with clock-associated cis-elements, suggesting circadian regulation of CAM. About 20% of pineapple microRNAs have diel expression patterns, with several that target key CAM-related genes. Expression and physiology data provide a model for CAM-specific carbohydrate flux and long-distance hexose transport. Together these resources provide a list of candidate genes for targeted engineering of CAM into C3 photosynthesis crop species.

KW - Ananas comosus

KW - CAM photosynthesis

KW - circadian regulation

KW - cis-element

KW - stomata

UR - http://www.scopus.com/inward/record.url?scp=85029595272&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85029595272&partnerID=8YFLogxK

U2 - 10.1111/tpj.13630

DO - 10.1111/tpj.13630

M3 - Article

C2 - 28670834

AN - SCOPUS:85029595272

SN - 0960-7412

VL - 92

SP - 19

EP - 30

JO - Plant Journal

JF - Plant Journal

IS - 1

ER -

Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple

Abstract

Funding

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this