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Molecular Mechanisms Affecting Cell Wall Properties and Leaf Architecture

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The Leaf: A Platform for Performing Photosynthesis

Summary

Leaf architecture is determined by cell shape, size, and density. As plant cells are enclosed by a rigid cell wall, changes to leaf architecture have to occur through downstream genetic systems that induce alterations in (1) cell wall composition, (2) synthesis, assembly, and orientation of cytoskeletal elements and/or (3) the degree of cross-linkage between wall components in response to upstream developmental and environmental cues. This chapter reviews how leaf architecture is influenced by molecular mechanisms that modulate the above wall modification processes. Upstream signaling systems such as salicylic (SA), jasmonic (JA), and gibberellic (GA) acid have significant effects on leaf architecture. GA promotes and JA and SA suppress growth. Leaf architectural changes are brought about by these upstream systems in concert or in an interactive manner, and the associated downstream molecular systems that are involved in executing changes to cell wall properties will be discussed. Evidence will be provided to show that xyloglucan endotransglucosylase/hydrolase and pectin methyltransferase/pectin methylesterase/pectin methylesterase inhibitor systems are key downstream execution points of leaf architectural changes common to different upstream molecular systems. Optimization of leaf architecture maximizes light interception, gas exchange properties, and photosynthesis. In addition, plant growth has been shown to be more sensitive to leaf area than to area-based photosynthesis rate. Therefore, understanding genes and molecular mechanisms that affect cell wall properties and leaf architecture has broader implications in terms of crop improvement, and candidate genes that can be manipulated to optimize leaf architecture in order to maximize net carbon assimilation and plant growth will be proposed.

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Abbreviations

ABA:

abscisic acid

ABP1 :

PUTATIVE AUXIN RECEPTOR AUXIN BINDING PROTEIN

AIR:

alcohol insoluble residue

AN :

ANGUSTIFOLIA

ARP2/3 :

ACTIN RELATED PROTEIN

BR:

brassinosteroids

BRICK1 :

SCAR/WAVE ACTIN-NUCLEATING COMPLEX SUBUNIT

C:

carbon

CAMTA :

CALMODULIN BINDING TRANSCRIPTION ACTIVATOR

CBF :

CRT/DRE BINDING FACTOR

CBP60G :

CALMODULIN BINDING PROTEIN 60G

CESA :

CELLULOSE SYNTHASE

CGR :

COTTON GOLGI-RELATED

cgr2com:

cgr2/3 complemented by CGR2

CGR2OX:

CGR2 overexpression line of Arabidopsis thaliana

CO2 :

carbon dioxide

CRT:

C-repeat

CSL :

CELLULOSE SYNTHASE LIKE

CYP85A1 :

BRASSINOSTEROID-6-OXIDASE

CYP90C1 :

CYTOCHROME P-450 FAMILY STEROID HYDROLASE

DELLA:

PIF transcription factor repressors

DRE:

dehydration responsive element

ER :

ERECTA

F-actin:

actin microfilaments

FR:

far-red

GA:

gibberellic acid

GT8 :

GLYCOSYL TRANSFERASE8

IAA:

auxin

ICS1 :

ISOCHORISMATE SYNTHASE

IIIe bHLHs:

basic helix-loop-helix subgroup IIIe transcription factors

JA:

jasmonic acid

JAZ:

jasmonate ZIM-domain repressors

jazQ:

JAZ quintuple mutation

LMA:

leaf dry mass per unit leaf area

LMD:

leaf mass density

LNG :

LONGIFOLIA

MAP18 :

MICROTUBULE ASSOCIATED PROTEIN18

MDP40 :

MICROTUBULE DESTABILIZING PROTEIN40

MF:

fine actin filament

MOR1 :

MICROTUBULE ORGANIZATION PROTEIN

MT:

microtubule

MYC2:

a basic helix-loop-helix transcription factor

NAP1 :

NCK-ASSOCIATED PROTEIN

nt:

nucleotide

PCR:

polymerase chain reaction

Pfr:

active form of phytochrome that absorbs far-red light

PHYB :

PHYTOCHROME-B

PIF:

phytochrome-interacting factors

PIN :

PIN-FORMED AUXIN EFFLUX CARRIER GENE FAMILY PROTEIN

PME :

PECTIN METHYLESTERASE

PMEI :

PECTIN METHYLESTERASE INHIBITOR

PMT:

pectin methyltransferase

Pr:

inactive form of phytochrome that absorbs red light

PVX:

potato virus X vector

QUA :

QUASIMODO

R:

red

RhoGAP:

negative regulator of ROP

RhoGEF:

Rho-guanine nucleotide exchange factors

RIC :

ROP-INTERACTIVE CRIB MOTIF PROTEIN

RNA-seq:

RNA sequencing

ROP :

RHO-RELATED GTPASE FROM PLANT (RhoGTPase)

ROT3 :

ROTUNDIFOLIA3

rubisco:

ribulose bisphosphate carboxylase oxygenase

SA:

salicylic acid

SARD1 :

SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1

SBP-BOX :

SQUAMOSA PROMOTER BINDING PROTEIN–LIKE GENE

S c :

chloroplast surface area facing intercellular air spaces per unit leaf area

SCAR :

SUPPRESSOR OF CYCLIC AMP RECEPTOR

sid2-1 :

salicylic acid induction-deficient 2-1

siRNA:

small interfering RNA

S mes :

mesophyll cell surface area facing intercellular air spaces per unit leaf area

SPIKE :

RHOGEF OR DOCK180-TYPE GUANINE NUCLEOTIDE EXCHANGE FACTOR

SRA1 :

RAC1-ASSOCIATED PROTEIN-1

TMK :

TRANSMEMBRANE KINASE SUBFAMILY OF RECEPTOR-LIKE KINASES

TSD2 :

TUMOROUS SHOOT DEVELOPMENT2

VIGS:

virus-induced gene silencing

VPDB:

Vienna-Pee-Dee Belemnite standard

WAVE :

WISKOTT–ALDRICH SYNDROME PROTEIN-FAMILY VERPROLIN HOMOLOGOUS PROTEIN

XEH :

XYLOGLUCAN ENDOHYDROLASE

XET :

XYLOGLUCAN ENDOTRANSGLUCOSYLASE

XTH :

XYLOGLUCAN ENDOTRANSGLUCOSYLASE/HYDROLASE

XXT :

XYLOSYLTRANSFERASE

δ13CVPDB :

ratio of 13C to 12C isotopes in leaf tissue relative to a Vienna-Pee-Dee Belemnite standard

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Acknowledgments

We are grateful to Drs. Sean E. Weise, (Department of Biochemistry and Molecular Biology), Cliff Foster (the Cell Wall Facility, Great Lakes Bioenergy Research Center), Alicia Withrow and Melinda Frame (Center for Advanced Microscopy) of Michigan State University (East Lansing, MI), and to Dr. Suvankar Chakraborty (Stable Isotope Ratio Facility for Environmental Research) of the University of Utah (Salt Lake City, UT) for their support. We also wish to thank Jim Klug and Cody Keilen (Growth Chamber Facility) of Michigan State University for their assistance and all members of the Brandizzi, Thomashow, Howe, and Sharkey labs for their support. Funding for this research was provided by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U. S. Department of Energy (award number DE-FG02-91ER20021) and in part by the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494). Partial salary support for MT, GH, TDS, and FB came from Michigan AgBioResearch.

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Weraduwage, S.M. et al. (2018). Molecular Mechanisms Affecting Cell Wall Properties and Leaf Architecture. In: Adams III, W., Terashima, I. (eds) The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration, vol 44. Springer, Cham. https://doi.org/10.1007/978-3-319-93594-2_8

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