Nitric Oxide in Plants Occurrence, Function and Use

Nitric Oxide in Plants Occurrence, Function and Use

by

Ya'acov Y. Leshem Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel

with the participation of

Jeng-Sheng Huang Department of Plant Pathology, North Carolina State University, Raleigh, North Carolina, U.S.A.

and

Dean Der-Syh Tzeng and Chun-Chi Chou Department of Plant Pathology, National Chung-Hsing University, Taichung, Taiwan, Republic of China

~.

" SPRINGER-SCIENCE+BUSINESS MEDIA, B.V.

A c.I.P. Catalogue record for this book is available from the Library of Congress.

ISBN 978-94-010-5840-7 ISBN 978-94-011-4239-7 (eBook) DOI 10.1007/978-94-011-4239-7

Printed on acid-free paper

Cover lllustration: Nitric oxide/ethylene stoichiometry in ripening strawberries -discussed in detail in Chapter Three.

AII Rights Reserved © 2000 Springer Science+Business Media Dordrecht Originally published by Kluwer Academic Publishers in 2000 Softcover reprint of the hardcover 1 st edition 2000 No part of the material protected by this copyright notice may be reproduced or utilized in any forrn or by any means, electronic or mechanical , incIuding photocopying, recording or by any information storage and retrieval system, without written permission from the copyright owner.

To my wife, Hasia, and the gang

Contents

Acknowledgements Abbreviations Glossary of nitrogen compounds mentioned in the text Colorplates

Part One: Endogenous Regulatory Processes

Xl

xv XVll

XIX

1. The Biological Conquest of Nitric Oxide 3 1. Introduction 3 2. NOS synthesis 4 3. NOS and the cytochrome P450 enzymes 5

3.1 Chemical control of NOS 6 4. Processes effected by NO in mammals 7

4.1 Promotory effects 7 4.2 Inhibitory andlor harmful effects 10

5. NO and peroxynitrites or Whodunit? 11 6. NO in plants 11

6.1 Promotory effects 11 6.2 Inhibitory effects of NO and of NOS-like activity 15

7. Conclusions and a future outlook 16 References 18

2. The Peroxynitrites 25 1. The Pryor-Squadrito pathway of peroxynitrite formation and

action 28 References 30

Vll

3. Nitric Oxide as an Endogenous Regulator of Fruit, Vegetable and Flower Maturation and Senescence 33

1. Overview of scientific rationale 33 2. Occurrence in higher plants 34 3. Interlinkage of NO and ethylene emission in senescing foliage 37

and in fruit, flower and vegetable rip'ening 3.1 NO and CzH4 stoichiometry in postharvest produce 40

4. Horticultural application of NO 41 5. Site(s) of NO synthesis in fruit maturation 46

5.1 Further sites of NO production 49 5.2 Differential response of climacteric and non-climacteric fruit 49

6. A case study: strawberry 50 6a. Storage and postharvest procedure 50 6b. Photo acoustic determination of endogenous NO/CzH4 52

stoichiometry 7. Photo acoustic spectroscopy (PAS) 53 8. Mode of action of NO in ethylene regulation 56

References 58

4. Nitric Oxide in Plant Pathology 63 1. Introduction 63 2. Nitric oxide concentrations and nitric oxide synthase 65

activities in plant-pathogen interactions 3. Nitric oxide and the hypersensitive reaction 69

3.1 Nitric oxide donors elicit hypersensitive-like symptoms 69 3.2 Nitric oxide synthase inhibitors comprise the hypersensitive

reaction 71 4. Nitric oxide and the phytoalexin production 72 5. Nitric oxide and the biosynthesis of pathogenesis-related

proteins 72 6. Nitric oxide and respiration 73 7. Nitric oxide and chlorophyll 75 8. Nitric oxide and nitrogen fixation 76 9. The nitric oxide-signaling pathway in plant-pathogen

interactions: A model 79 10. Future prospects 80 11. Acknowledgement 81

References 81

viii

5. Plant Antecedents of, and Analogy to Viagra 87 1. Cyclic nucleotides in biological regulation 88

1.1 a. General: the 'second messenger' concept of hormonal action 88 Ovulation and cAMP 90

1.2 b. Cyclic nucleotides in plant growth regulation 92 1.2.i. Auxins 92 1.2.ii. Gibberellins 93 1.2.iii. Cytokinins 94

2. The turn of the (nucleo-)tide: advent of cGMP 96 3. The regulative physiology of sildenafil (Viagra) 98 4. Does Viagra act on plants? 100 5. A caveat and word of precaution 102

References 103

Part Two: Atmospheric Nitric Oxide and Plant Growth

6. Nitrogen Oxides in the Environment: Benign and Harmful Biological Effects of Atmospheric NO 111

1. Nitrogen oxides - N02 and NO in the troposphere 111 2. Nitrous oxide (N20, "laughing gas") 114 3. N20 effects on ripening and senescing climacteric fruits 116 4. Direct atmospheric nitric oxide fixation by higher plants 117 5. Nitrite reductase 119 6. Harmful effects of NO 121

6.1 NO pollution and the photosynthetic apparatus 121 6.2 Phytosanitary effects of NO on photosynthesis-related

processes 128 6.3 Toxic chemical species which may be generated by NO in

plants 128 6.3.1. Formation of dinitrosyl iron species within key

enzymatic species 128 6.3.2. Auto-oxidation processes 130 6.3.3. NO reaction with superoxide (02-) to form 130

peroxynitrite 7. References 131

ix

7. Is Nitric Oxide a Component ofthe GAS (General Adaptation Syndrome) Mechanism in Plant Stress Coping? 137

1. The GAS syndrome and stress 137 2. Supportive data 140 3. NO and ozone stress 142

3.1 Plant NO as an inducer of 0 3 142 References 143

8. Epilogue 147

Index 151

x

Acknowledgements

This text endeavors to present a cogent bird's-eye view of what may be considered a groundbreaking field in basic plant physiology. Its compilation is the combined result of cooperative research between several laboratories the world over, as well as of incorporation of information attained from isolated research teams that have come up with novel ideas. No less than to faculty, colleagues and research scientists in various institutes, I am indebted to many of my students who have played an active part in the overall effort.

Special thanks are due to the erstwhile Dean Prof. Haim Breitbart and to the late Professor Yehouda Levy, Head of the Life Sciences Department of the Bar-Ilan University, who provided encouragement and initial funding for launching the plant-NO project. Ongoing aid has been obtained from the Research Council of Bar-Ilan University.

It has been a pleasure and a privilege to spend periods of cooperative research with Prof. Ron Wills and Vivian Ku at the Department of Food Technology, University of Newcastle, Ourimbah, Australia. Drs. Frans Harren and Luc-Jan Laarhoven kindly enabled access to the photoacoustic spectrometry laboratory at the Trace Gas Facility, Department of Molecular and Laser Physics, University of Nijmegen, The Netherlands. Prof. Shimshon Ben Yehoshuah, Department of Postharvest Science, The Volcani Agricultural Research Center, Beit Dagan, Israel, has followed our project throughout and his constructive criticism and the follow-up of which, has contributed to several of the issues broached in Chapter 3. Prof. Alan Wellbum, Institute of Environmental Studies, University of Lancaster, U.K. and Dr. Antje Eickriede, Institute of Geospheric Chemistry and Dynamics, JUlich, Germany, provided me with a wider insight to environment-associated NO effects on plants.

In particular I am indebted to Prof. J.-S. Huang and Profs. D.D.-S. Tseng and c.-C. Chou from the Departments of

xi

Plant Pathology, respectively from the North Carolina State University, U.S.A. and the University of Taiwan, for their meaningful Chapter 4 of this book dealing with the role of NO in plant pathology and disease resistance.

Colleagues from various universities and research organizations whose names and institutional affiliations are mentioned in the captions of pertinent diagrams, have kindly provided illustrative material. For their helpful discussions and exchange of ideas, I am indebted to Prof. H.K. Lichtenthaler, the Botanical Institute, University of Karlsruhe, Germany, Prof. PJ.c. Kuiper, the Biological Center, Haren, University of Groningen, and Prof. Rens Voesenek, Department of Ecology, University of Utrecht - both from the Netherlands, Brian Day, Campden and Chorleywood Food Research Association, Gloucertershire, U.K., Dr. M. Delledonne, Plant Biology Laboratory, The Salk Institute, La Jolla, California; Dr. A. Levin of the Life Sciences Institute of the Hebrew University, Jerusalem. Israel, Prof. Erich Elstner of the Technical University, Munich, Germany and Prof. lC. Pech, ENSAT, INRA, France. Prof. Alex Tsafriri of the Weizmann Institute, Rehovoth, Israel, provided invaluable information on the involvement of NO in human procreation and its connection with cyclic nucleotide metabolism. Amongst my many students who have participated in the effort, especial mention is made of Esther Haramaty, Yulia Pesachov and David Bar-Golan, who carried out key experiments that lent further credence to the original experimental hypothesis of occurrence and function of NO in higher plants.

I furthermore express my deepest thanks to Dr. Lev Shvidel and Dr. Joshua Friedman, Kupat Holim Medical Center, Rehovoth, Israel, due to whom this text took considerably longer to write than originally planned but without whom would probably not have been written at all.

Especial thanks are due to Sharon Victor and Avrille Goldreich of the English Secretariat of Bar-Ilan University's Life

xu

Sciences Faculty - to Sharon for her patient and meticulous typing, retyping and arrangement of the text, and A vrille, for her adept rendering of the manuscript into a print-ready format and to Tamir Castiel for his invaluable aid in setting the diagrams. Finally, I express my gratitude to Ir. Adriaan C. Plaizier, Head and Editor of the Biosciences Division of the Kluwer Academic Publishing House, to his assistant Noeline Gibson and Dr. J.N. Flipsen, Publishing Editor, Biosciences Unit and his assistant Gloria Verhey for their staunch encouragement and aid throughout the production of this text.

And now a word to the gentle reader: a special endeavor has been made to accompany the main body of the text with manifold self-explanatory diagrams and several color diagrams. This, together with the annotated bibliographies to each chapter, will hopefully encourage the reader - both novice and initiate -to delve deeper into, and suggest solutions to some of the problems still facing the mode of action in plants of the fascinating nitric oxide molecule which recently has been designated as "biochemistry's new superstar."

Ya'acov Y. Leshem

xiii

Abbreviations

ABA ACC ACO ACS cAMP carboxy-PTIO

cGMP CK DGDE DETC 2,4-DNP EDRF EPR FAD FMN GA GAS GTP HO·

HR HSP IAA Lb MAP MAPK

abscisic acid l-aminocyclopropane-I-carboxylic acid ACC oxidase (= EFE ethylene forming enzyme) ACC synthase cyclic adenosyl monophosphate carboxy-2-phenyl-4,4,5,5-tetramethylimidazoline-I-oxyl-3-oxide cyclic guanosyl monophosphate cytokinin digalactosyldiacylglyceride diethyldithiocarbamic acid 2,4-Dinitrophenol endothelium derived relaxing factor electron paramagnetic resonance flavin adenine dinucleotide flavin mononucleotide gibberellic acid general adaptation syndrome guanosine 5'-triphosphate hydroxyl free radical

hypersensitive reaction heat shock protein indole acetic acid leghemoglobin modified atmosphere packaging mitogen activated protein kinase

xv

mep MGDG NMA, L-NMMA, orN-ARG NOC-18

PBN PDE PMN ppbv PRproteins PTIO

ROS SAM SDS-PAGE

SHAM Sin-1 SNAP SNP TMV Tris-HCI buffer

1-methylcyclopropene monogalaetosyldiaeylglyceride

NG -methyl-L-arginine 1-hydroxy-2-oxo-3 ,3-bis(2-aminoethyl)-1-triazene

. superoxide

photoaeoustie spectroscopy S,S'-1 ,3-pheny~ene-bis(1 ,2-ethanediyl)­bis-isothiourea phenyl N-tert-butylnitrone phosphodiesterase polymorphonuclear leucocytes parts per billion by volume pathogenesis-related proteins 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide reactive oxygen species S-adenosylmethionine sodium dodecyl sulfate polyacrylamide gel electrophoresis salieylhydroxamic acid 3-morpholinosydnonimine S-nitro so-N -acety lpenicillamine sodium nitroprusside tobacco mosaic virus tris(hydroxy)aminomethane HCI buffer

XVI

Glossary of nitrogen compounds mentioned in the text

Lb-NO NaR NO, NO· N02

N02•

N20 N203 NOS NOx

ONOO­ONOOH

nitrosylleghemoglobin nitrate reductase nitric oxide or nitrogen monoxide nitrogen dioxide nitrogen dioxide free radical nitrous oxide dinitrogen trioxide nitric oxide synthase nitrogen oxides (NO and N02)

peroxynitrite peroxynitrous acid

xvii

Colorplate 1 (see also p. 41)

A

B b c d b

, .... . -: . ... - ':,:.

, ," i <"..,. . ,'~., .....

a

Colorplate 2 (see also p" 45)

Coiorpiate 3A (see also p. 70)

Coiorplate 3B (see also p. 70)

cGMP·depcOOcnt ptOlcJn klna':tCs and pnoc;phodl~lcra'\C'S

cGMP.galed "'" channels

tGMP \\ ...

GTP " Jasmoni<;.....-- Ir. ....... ~""?=""""'=:11 aCId I

ONA

EnzymOS f()( p!>ytooklxln and PR protein bioSyntheSis and

cell wan rortJhCauon======*====l==========~

PLASMA MEMBRANE

Colorplate 4A (see also p. 78)

I-I u:-.t lanl

Nodule

co,

CYTOSOL

0, r, ~11"~'OH."'.II"o\lr.;

""'~IQn.t..

INFECTED CEt!,

Colorplate 4B (see also p. 78)

Colorplate 5 (see also p. 101)

Colorplate 6 (see also p. 115)

Conlral

f~-'~' I,(:c 0 .. <10 ~I

H. ' J -[ tl n 1-

'" ,i. '1 ~ [. . , .

f, I c I ;) If

I I.. . >- H ... .) -t~: .. .0 11 .. ' I \ . ; ,1 I I' ~

\. \I'

( ..• , /' ~, . 11.1 ~~ . I ..,

u \ ~ . ~ I c ... ' I I ,. \. u ~\ I ! '" ... ~. ·1 (; d, -.2

P I \I . I ' ! ~ : ..... .J

. / T"'" i' --1" -

->'- 1 i" - - I

~6f1 bUt {Il'" ll H ,j(,(J J! } nm

Coiorpiate 7 (see also p. 127)

o <Xl ~ -~

NOUl91HNI e-o Q

O~!) ~"ll't1i:;J~ u