Plant Virus-Host Interaction: Molecular Approaches and Viral Evolution

Plant Virus-Host Interaction: Molecular Approaches and Viral Evolution, Second Edition, provides comprehensive coverage of molecular approaches for virus-host interaction. The book contains cutting-edge research in plant molecular virology, including pathogenic viroids and transport by insect vectors, interference with transmission to control viruses, synergism with pivotal coverage of RNA silencing, and the counter-defensive strategies used by viruses to overcome the silencing response in plants. This new edition introduces new, emerging proteins involved in host-virus interactions and provides in-depth coverage of plant virus genes’ interactions with host, localization and expression.

With contributions from leading experts, this is a comprehensive reference for plant virologists, molecular biologists and others interested in characterization of plant viruses and disease management.

• Introduces new, emerging proteins involved during the host-virus interaction and new virus strains that invade new crops through recombination, resorting and mutation
• Provides molecular approaches for virus-host interaction
• Highlights RNA silencing and counter-defensive strategies for disease management
• Discusses the socioeconomic implications of viral spread and mitigation techniques

• Language: English
• Publisher: Academic Press
• Release date: Jan 12, 2021
• ISBN: 9780128244838

Book preview

Plant Virus-Host Interaction

Molecular Approaches and Viral Evolution

Second Edition

Rajarshi Kumar Gaur

Professor, Department of Biotechnology, Deen Dayal Upadhyaya Gorakhpur University, Gorakhpur, Uttar Pradesh, India

S.M. Paul Khurana

Professor, Amity Institute of Biotechnology, Amity University-Haryana, Manesar, Gurugram, Haryana, India

Pradeep Sharma

Principal Scientist (Biotechnology), Division of Crop Improvement, ICAR— Indian Institute of Wheat and Barley Research (IIWBR), Karnal, Haryana, India

Thomas Hohn

Institute of Botany, University of Basel, Basel, Switzerland

Table of Contents

Cover image

Title page

Copyright

Contributors

About the editors

Foreword

Preface of the first edition

Preface of the second edition

Section A: Plant virus-host interaction

Chapter 1: Host-encoded miRNAs in plant-virus interactions—What's new

Abstract

1: Introduction

2: miRNAs in PTI—Antiviral RNA-silencing pathway

3: miRNAs in ETI

4: miRNAs in host susceptibility

5: Symptom related miRNAs

6: Cultivar-specific miRNAs

7: miRNAs in transgenic virus resistant plants

8: Plant miRNAs directly targeting the virus genome for cleavage

9: Multiple novel regulatory layers of miRNAs

Chapter 2: Plant nonhost resistance against viruses: Current status and future prospects

Abstract

Acknowledgments

1: Introduction

2: RNA silencing as a determinant of antiviral NHR

3: NHR due to incompatible interaction between viral and host factors

4: NHR mediated by host inhibitors

5: Cell wall (CW)–plasma membrane (PM)–cytoskeleton-associated antiviral NHR

Chapter 3: Viral movement-cellular protein interaction

Abstract

1: Introduction

2: Movement of virus within plant

3: Viral movement proteins

4: Techniques to study virus-host interactions

5: Conclusion and future perspectives

Chapter 4: Virus latency: Heterogeneity of host-virus interaction in shaping the virosphere

Abstract

Acknowledgments

1: Introduction

2: Diversity and biology of latent plant viruses and viroids

3: Interactions of latent plant viruses and viroids within virosphere

4: Transition from latency to activation

5: Latency in animal systems

6: Horizontal virus transfer and cross kingdom infection

7: Conclusion and outlook

Chapter 5: Functional biology of potato-virus interactions

Abstract

1: Potato

2: Potato viruses

3: Genome organization of important potato viruses

4: Strains of major potato viruses

5: Molecular mechanism of resistance to potato viruses

6: Host susceptibility factor/recessive resistance

7: Changes in gene expression-transcriptome and proteome analysis

8: Heat shock proteins in potato-virus interactions

9: Involvement of hormones in potato-virus interactions

10: Virus induced gene silencing for functional analysis

11: Virus-derived small interfering RNAs (vsiRNAs)

12: Host recovery phenomenon

13: Cytopathological changes in cell organelles

14: Facilitating and antagonistic interactions of potato viruses

15: Conclusion

Chapter 6: Virus-host interactome of Potyviridae

Abstract

1: Introduction

2: Interaction for virus movement

3: Interaction to escape from host defense

4: Interaction with chloroplast

5: Interaction for viral replication and translation

6: Interaction with chaperones for proper viral protein folding

7: Interaction for post-translational modification

8: Conclusion

Chapter 7: Geminiviruses and their interaction with host proteins

Abstract

1: Geminiviruses

2: Classification of geminiviruses

3: Satellite molecules associated with begomoviruses

4: Geminivirus encoded proteins and their interaction with host proteins

Chapter 8: Factors controlling the fate of tomato yellow leaf curl virus (TYLCV) in its vector, the whitefly vector Bemisia tabaci

Abstract

Acknowledgments

1: Introduction

2: Tomato yellow leaf curl viruses vectored by the whitefly Bemisia tabaci complex

3: TYLCVs accumulating in B. tabaci during feeding on infected plants rapidly reach optimal amounts, even though the insect continues to feed

4: TYLCVs translocate in the B. tabaci organs and cells mediating begomovirus circulative transmission, but not only

5: Most of the ingested virus accumulates in the digestive tract; only a tiny fraction reaches the salivary glands

6: Slow decline in the begomovirus amounts and of infectivity after insects ceased feeding on infected plants

7: How many virions has a whitefly to ingest before it is able to infect a tomato plant?

8: Stability and changes of the begomovirus genome in B. tabaci

9: Processes that affect the amount of virus in the whitefly

10: Differential virus transmission capacities

11: Role of endosymbionts in modulating levels of begomoviruses

12: Candidate genes controlling the amount of virus in whiteflies and virus transmission to plants

13: Adaptation of whitefly invasive species to new viruses

14: Conclusions and perspectives

Chapter 9: The interaction between begomoviruses and host proteins: Who determines the pathogenicity of begomoviruses

Abstract

1: Introduction

2: Genomic organization

3: Viral genes and proteins

4: Plant proteins to combat the viral infection

5: Encounter between host proteins and geminivirus proteins

6: Mixed interactions

7: Conclusion

Chapter 10: Multifunctional role of 2b protein in pathogenesis of the viruses under the family Bromoviridae

Abstract

1: Introduction

2: 2b protein in the genus Cucumovirus

3: 2b in ilarvirus

4: Concluding remarks and perspectives

Section B: Plant virus evolution and diversity

Chapter 11: Evolution and diversity of plant RNA viruses

Abstract

1: Introduction

2: Mechanisms of evolution of RNA viruses

3: Population size, specificity and host range

4: Role of insects in viral evolution

5: Phylogeny of RNA viruses

6: Conclusions

Chapter 12: Plant virus: Diversity and ecology

Abstract

1: Introduction

2: Vector dynamics in plant virus ecology

3: Host dynamics in plant virus ecology

4: Conclusions

Section C: Plant virus management

Chapter 13: Molecular biology of antiviral arms race between plants and viruses

Abstract

1: Introduction

2: RNA silencing acts as defense mechanism targeting plant viral nucleic acids

3: Viral suppressors of RNA silencing (VSRs)

4: Pathogen-derived virus resistance

5: RNAi-mediated virus resistance

6: Conclusion

Chapter 14: Control of plant pathogenic viruses through interference with insect transmission

Abstract

Acknowledgments

1: Introduction

2: Modes of transmission

3: Main groups of insect vectors of plant viruses

4: Control of insect vectors to control virus diseases

5: Interference with transmission

6: Conclusion

Chapter 15: Small RNA-mediated begomoviral resistance in plants: Micro in size but mega in function

Abstract

1: Introduction

2: Classification

3: General characteristics

4: Genome organization of begomoviruses

5: Roles of individual genes of begomovirus and associated satellites

6: RNA interference-mediated resistance

7: Summary and conclusion

Chapter 16: Managing chili leaf curl disease through RNAi based strategies

Abstract

1: Introduction

2: Host plant resistance to the virus

3: Conclusion

Chapter 17: CRISPR/Cas9: A magic bullet to deal with plant viruses

Abstract

1: Introduction

2: CRISPR: A prokaryotic safeguard mechanism to defend intruders

3: CRISPR/cas9 for editing plant genome

4: Drawbacks of the CRISPR/Cas9 system

5: Advantages of CRISPR/Cas9 technology

6: Prime editing for precise genome editing: Way forward

7: Conclusion and future perspective

Chapter 18: Evaluation of the reaction of cereal cultivars to viruses as a preliminary step in plant health management

Abstract

1: Viruses as permanent danger for cereal crops

2: Evaluation of the risk as a request for safety of cereals

3: Methods

4: Conclusions

Chapter 19: Ecological methods to control viral damages in tomatoes

Abstract

1: Tomatoes as an important valuable food

2: Diseases of tomatoes with an emphasis on viral diseases

3: Ecological methods for control of tomato viruses

Chapter 20: Overcoming limitations of resistance breeding in Carica papaya L. against papaya ringspot virus—Recent approaches

Abstract

1: Introduction

2: Papaya ringspot virus

3: Present strategies for PRSV management

4: Breeding PRSV resistant papaya cultivars

5: Recent developments

6: Conclusion and future prospects

Chapter 21: Diversity analysis of begomoviruses infecting papaya and its mechanisms of resistance

Abstract

Acknowledgments

1: Introduction

2: Diversity and distribution of begomoviruses infecting papaya in India

3: Resistance mechanisms for the control of begomovirus

4: Conclusion

Chapter 22: Plant viruses as an engineered nanovehicle (PVENVs)

Abstract

Acknowledgment

Declaration of competing interest

1: Introduction

2: Synthesis of plant virus-Based engineered nanovehicles (PVENVs)

3: Basic features and applications of plant viruses and bacteriophages as PVENVs

4: Conclusion

Index

Copyright

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Contributors

Numbers in parenthesis indicate the pages on which the authors' contributions begin.

Nasim Ahmed 191     National Institute for Biotechnology and Genetic Engineering (NIBGE), Faisalabad, Pakistan

Imran Amin 191     National Institute for Biotechnology and Genetic Engineering (NIBGE), Faisalabad, Pakistan

Shamresh Anand 267     Department of Biotechnology, Deen Dayal Upadhyay Gorakhpur University, Gorakhpur, Uttar Pradesh, India

Surabhi Awasthi 303     National Botanical Research Institute, Lucknow, India

Mirza S. Baig 383     Plant Virus Laboratory, Department of Biosciences, Jamia Millia Islamia, (A Central University), New Delhi, India

S.K. Chakrabarti 139     ICAR-Central Potato Research Institute, Shimla, Himachal Pradesh, India

Ornela Chase 359     Centre for Research in Agricultural Genomics CRAG, CSIC-IRTA-UAB-UB, Barcelona, Spain

Reshu Chauhan 303     National Botanical Research Institute, Lucknow, India

Xiaofei Cheng 45     College of Agriculture, Northeast Agricultural University; Key Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region of Chinese Education Ministry, Harbin, China

Gilbert Nchongboh Chofong 111     Julius Kühn Institute (JKI)-Federal Research Center for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany

Henryk Czosnek 231     Institute of Plant Sciences and Genetics in Agriculture, Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

Daliyamol 283     Advanced Centre for Plant Virology, Division of Plant Pathology, Indian Agricultural Research Institute, New Delhi, India

Filza Fatma 267     Department of Biotechnology, Deen Dayal Upadhyay Gorakhpur University, Gorakhpur, Uttar Pradesh, India

Inmaculada Ferriol 359     Centre for Research in Agricultural Genomics CRAG, CSIC-IRTA-UAB-UB, Barcelona, Spain

R.K. Gaur 267, 443, 469, 525     Department of Biotechnology, Deen Dayal Upadhyay Gorakhpur University, Gorakhpur, Uttar Pradesh, India

Murad Ghanim 231     Department of Entomology, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel

Rena Gorovits 231     Institute of Plant Sciences and Genetics in Agriculture, Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

Om Prakash Gupta 443     Biotechnology Unit, ICAR-Indian Institute of Wheat and Barley Research, Karnal, Haryana, India

Aradhana Lucky Hans 507     Department of Biotechnology, School for Bioscience and Biotechnology, Babasaheb Bhimrao Ambedkar University (A Central University), Lucknow, Uttar Pradesh, India

D. Michael Immanuel Jesse 319     Department of Biotechnology, St. Joseph's College (Autonomous), Tiruchirappalli, India

Tennyson Jebasingh 169     Department of Plant Sciences, School of Biological Sciences, Madurai Kamaraj University, Madurai, Tamil Nadu, India

A. Jeevalatha 139     ICAR-Indian Institute of Spices Research, Kozhikode, Kerala, India

Hira Kamal 191     National Institute for Biotechnology and Genetic Engineering (NIBGE), Faisalabad, Pakistan

K. Kathiravan 319     Plant Molecular Virology Laboratory, Department of Biotechnology, University of Madras, Chennai, India

Jawaid A. Khan 383     Plant Virus Laboratory, Department of Biosciences, Jamia Millia Islamia, (A Central University), New Delhi, India

S.M. Paul Khurana 59, 139     Amity Institute of Biotechnology, Amity University, Manesar, Gurugram, Haryana, India

Kappei Kobayashi 283     Plant Molecular Biology and Virology, Graduate School of Agriculture, Ehime University, Matsuyama, Ehime, Japan

R. Vinoth Kumar 331     National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bengaluru, Karnataka, India

Juan José López-Moya 359     Centre for Research in Agricultural Genomics CRAG, CSIC-IRTA-UAB-UB, Barcelona, Spain

Yameng Luan 45     College of Agriculture, Northeast Agricultural University, Harbin, China

Bikash Mandal 283     Advanced Centre for Plant Virology, Division of Plant Pathology, Indian Agricultural Research Institute, New Delhi, India

Shahid Mansoor 191     National Institute for Biotechnology and Genetic Engineering (NIBGE), Faisalabad, Pakistan

Avinash Marwal 525     Department of Biotechnology, Mohanlal Sukhadia University, Udaipur, Rajasthan, India

Janos Minarovits 111     Department of Oral Biology and Experimental Dental Research, University of Szeged, Szeged, Hungary

Megha Mishra 267     Department of Biosciences, School of Liberal Arts, and Sciences, Mody University of Science and Technology, Sikar, Rajasthan, India

Neeti Sanan Mishra 419     Plant RNAi Biology Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India

Ritesh Mishra 507     Department of Biotechnology, School for Bioscience and Biotechnology, Babasaheb Bhimrao Ambedkar University (A Central University), Lucknow, Uttar Pradesh, India; Institute of Plant Sciences and Genetics in Agriculture, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

S.U. Mohammed Riyaz 319     Department of Biotechnology, Bharathidasan University, Tiruchirappalli, India

Sunil Mukherjee 283     Advanced Centre for Plant Virology, Division of Plant Pathology, Indian Agricultural Research Institute, New Delhi, India

Raghvendra Pratap Narayan 303     Netaji Subhash Chandra Bose Government Girls PG College Aliganj, Lucknow, India

Nikolay Petrov 469     New Bulgarian University, Sofia, Bulgaria

Ved Prakash 331     School of Life Sciences, Jawaharlal Nehru University, New Delhi, India

Devendran Ragunathan 331     School of Life Sciences, Jawaharlal Nehru University, New Delhi, India

Katja R. Richert-Pöggeler 111     Julius Kühn Institute (JKI)-Federal Research Center for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany

Anirban Roy 283     Advanced Centre for Plant Virology, Division of Plant Pathology, Indian Agricultural Research Institute, New Delhi, India

Anurag Kumar Sahu 419     Plant RNAi Biology Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India

Elangovan Sangeetha 169     Department of Plant Sciences, School of Biological Sciences, Madurai Kamaraj University, Madurai, Tamil Nadu, India

Sangeeta Saxena 507     Department of Biotechnology, School for Bioscience and Biotechnology, Babasaheb Bhimrao Ambedkar University (A Central University), Lucknow, Uttar Pradesh, India

Pradeep Sharma 267, 443     Biotechnology Unit, ICAR-Indian Institute of Wheat and Barley Research, Karnal, Haryana, India

Sunil K. Sharma 489     ICAR-Indian Agricultural Research Institute, Pune, India

Dinesh Kumar Singh 267     Department of Biotechnology, Deen Dayal Upadhyay Gorakhpur University, Gorakhpur, Uttar Pradesh, India

Garima Singroha 443     Biotechnology Unit, ICAR-Indian Institute of Wheat and Barley Research, Karnal, Haryana, India

Antoniy Stoev 461     Nikola Poushkarov Institute for Soil Science, Agrotechnology and Plant Protection, Sofia, Bulgaria

Mariya Stoyanova 469     Institute of Soil Science, Agrotechnologies and Plant Protection (ISSAPP) N. Pushkarov, Sofia, Bulgaria

Savarni Tripathi 489     ICAR-Indian Agricultural Research Institute, Pune, India

Priyanka Varun 507     Department of Biotechnology, School for Bioscience and Biotechnology, Babasaheb Bhimrao Ambedkar University (A Central University), Lucknow, Uttar Pradesh, India

Rakesh Kumar Verma 267     Department of Biosciences, School of Liberal Arts, and Sciences, Mody University of Science and Technology, Sikar, Rajasthan, India

Xiaoyun Wu 45     College of Agriculture, Northeast Agricultural University; Key Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region of Chinese Education Ministry, Harbin, China

Dinesh Kumar Yadav 59     Department of Botany, University of Allahabad, Prayagraj, Uttar Pradesh, India

Neelam Yadav 59     Department of Botany, University of Allahabad, Prayagraj, Uttar Pradesh, India

Sarika Yadav 59     Department of Biochemistry, Sri Venkateshawara College, University of Delhi, New Delhi, India

Zhimin Yin 3     Plant Breeding and Acclimatization Institute—National Research Institute, Młochów Research Center, Młochów, Poland

About the editors

Prof. (Dr.) Rajarshi Kumar Gaur is Professor in the Department of Biotechnology, Deen Dayal Upadhyaya Gorakhpur University, Gorakhpur, Uttar Pradesh, India. He completed his PhD from Chhatrapati Shahu ji Maharaj University, Kanpur, India, on molecular characterization of sugarcane viruses, viz., mosaic, streak mosaic, and yellow luteovirus. He received MASHAV fellowship of the Israel government in 2004 for his postdoctoral studies and joined the Volcani Centre, Israel and BenGurion University, Negev, Israel. In 2007, he received the Visiting Scientist Fellowship from Swedish Institute Fellowship, Sweden, to work in the Umeå University, Umeå, Sweden, and received a postdoctoral fellowship from ICGEB, Italy in 2007–08. He has made significant contributions on sugarcane viruses and published 130 national/international papers, authored 17 edited books, and presented nearly 50 papers in national and international conferences. He was honored as Fellow of Linnean Society in 2014, Fellow of Royal society of Biology in 2015, and Fellow of Society of Plant Research in 2016. He has bagged many other awards such as Prof. B.M. Johri Memorial Award, Society of Plant Research (SPR); Excellent Teaching Award by Astha Foundation, Meerut; UGC Research Teacher Award; Young Scientist Award in 2012 in biotechnology by the Society of Plant Research (SPR), Meerut; and Scientific and Applied Research Centre Gold Medal Award in 2011 for outstanding contributions in the field of biotechnology. He has visited several laboratories of the United States, Canada, New Zealand, the United Kingdom, Thailand, Sweden, and Italy. He has guided nine PhD students and bagged six projects funded by the Government of India including Indo-Bulgarian Bilateral projects. Currently, he is handling many national and international grants and international collaborative projects on plant viruses and disease management.

Prof. (Dr.) S M Paul Khurana received his PhD in 1969 and completed postdoctoral research in advanced virology at Kyushu University, Japan (1970–72), University of Minnesota, St Paul (United States, 1987–88) specializing in immunodiagnostics. He is currently Professor of Biotechnology and Head, University Science Instrument Centre, Amity University, Haryana, Gurgaon. Earlier he served as the vice-chancellor of Rani Durgavati University, Jabalpur during 2004–09; Project Coordinator AICRP (Potato) during 1994–2004; Director, Central Potato Research Institute, Shimla, during 2002–04; the Founder Director, Amity Institute of Biotechnology, Gurgaon, Haryana, during 2010–16; Dean, Science, Engineering and Technology during 2013–16; and Consultant CIP/FAO, during 1992, 1996, 1997. He has been invited/deputed to many international conferences, in India/abroad by the GOI/ICAR/UGC in the United Kingdom, United States, Netherlands, Canada, China, France, Greece, Japan, Malaysia, Thailand, Italy, Peru, South Africa, and Uganda; convened the Global Conference on Potato in New Delhi (December 6–9, 1999). He is also Advisor to NextOmics, Australia; Director, STEPS International (Greece, United States) Foundation (India Program, 2015–17) etc. He has bagged 40 + awards/honours including CPRI Golden Jubilee Outstanding Achievement award, 2000; National Environmental Science Academy Best Scientist of the Year Award 2002; CPRI S. Ramanujam Memorial Award, 2003; Ch. Devi Lal outstanding AICRP Award, 2005; UNO Dr S Radhakrishnan International Award for Excellence in Higher Education Management, 2006; ISCA Platinum Jubilee (Lecture) Award, 2010; ISMPP Lifetime Achievement Award, 2012; HSI Shivshakthi Lifetime Achievement Award, 2013; Eminent Scientist Honour: ISCA Sir JC Bose Medal, 2013; CHAI Honorary Fellowship and Lifetime Achievement Award, 2016; ISMPP Prof YL Nene Outstanding Teacher of Plant Pathology, 2018; IVS KS Bhargava Award for Eminent contributions to Virology, 2018; International Award for Excellence recognizing eminent contributions to promotion of significant research in medicinal and aromatic plants, at the 7th GOSMAP, Thailand, 2018; and KUD and ISMPP Award of Honour for Excellence in Research, 2019, etc. He is also Fellow of National Academy of Agriculture Sciences, National Academy of Biological Sciences etc.; Mentor World Society of Virology, 2016–19; And was Chair for RACs of three and QRTs of three ICAR Research Institutes. He has 55 years of research in pathology, virology, biotechnology on plant viruses on the detection and transmission and control for maintaining seed health and pioneered cloning of PVY/PLRV-CP genes and developed tobacco/potato transgenics with PVY-CP gene. He has published 235 + research papers, 125 reviews/book chapters, authored and edited 24 books (including that from Haworth Food Press, CRC Press, Elsevier, and Springer-Nature). He has guided 16 PhDs. He is currently editing a series of four books on biotechnology for Springer and Elsevier as well as two textbooks.

Dr. Pradeep Sharma is Principal Scientist (Biotechnology) at the ICAR-Indian Institute of Wheat and Barley Research Institute, Karnal, India. He received his PhD in 2002 with Prof N. Rishi, Research Associate (2002–05) at HPKV Palampur and HAU, Hisar Post-Doctoral Research (2006–08) at Tohoku University, Japan, with Prof M Ikegami as JSPS fellow. He also completed his postdoctoral work at ARO Volcani Center, Israel, with Prof Y Gafni (2006–07) and was DST Scientist (2006), Visiting Scientist at South Dakota State University (2011) and Oklahoma State University (2016). Dr. Sharma has made significant contributions on genomics of wheat, decoded Karnal bunt genomes, developed markers for both abiotic and biotic stresses in wheat, and also cloned several viral diseases from South East Asia and RNAi; published more than 110 national and international research papers, 25 invited chapters, and 08 scientific review articles; and edited seven books on biotic and abiotic stresses including RNAi technology. Dr. Sharma was conferred the Young Scientist’s Award (biannual 2005–06) of the National Academy of Agricultural Sciences and the Pran Vohra Award (2008–09) of the Indian Science Congress Association, Fellow of National Academy of Biological Sciences (2015), Fellow of Indian Virological Society (2012), and Fellow of Society for Advancement of Wheat and Barley Research (2019). He has worked at and visited many pioneering laboratories of the United States, the United Kingdom, Japan, France, China, the Netherlands, Indonesia, Turkey, and Israel.

Prof. (Dr.) Thomas Hohn is Professor Emeritus at the Botanical Institute, University of Basel. He is an Austrian, studied at the Max-Planck Institute, Tübingen, and has performed postdoctoral studies in Stanford, California. He was junior group leader at the Bicocenter of the University of Basel and group leader at the Friedrich Miescher Institute, Basel. His interests are in virology, originally in bacteriophages; he has studied self-assembly of small bacteriophages as well as morphogenesis of bacteriophage λ. The latter work, performed together with his wife, led to DNA-packaging. Later he shifted to plant viruses, where he recognized the first plant pararetrovirus (CaMV) and detected special viral translation strategies. Recently he became interested in the topic of RNA-interference and transgenesis. He has published more than 200 papers so far. For several years he has been involved together with his wife Barbara in the Indo-Swiss Collaboration in Biotechnology project, working together with Indian scientists to apply biotechnology for the improvement of pulses (Leguminosae) and cassava for use by subsistence farmers.

Foreword

Jeanmarie Verchot, Scientist, TAMU, USA

When I began my professional career studying plant viruses during my PhD studies in 1991, there was a revolution in creating infectious cDNA copies to inoculate plants, my own were to uncover the function of the potyvirus P1 protein. Research tools have advanced to include real time PCR, visual reporters like GFP and iLOV, confocal microscopy, computational studies, epigenetics and forward genetics to uncover host genes that contribute to infection or immunity. These advanced technologies led to the rapid and recent development of the field of Plant Virus-Host Interactions. I am excited for this second edition of your book Plant Virus-Host Interactions covering most recent advances in studying molecular approaches and virus evolution.

This book captures multiple and exciting dimensions of plant virus-host interactions with a clear focus on plant virus evolution and ecology. It is important to understand that viruses not only cause diseases in agricultural crops, but also exist in the natural ecosystem and may influence competition between plant species as well as insect populations outside of crop systems. This multi-authored book is a collection of 22 reviews on selected areas of plant viruses that have received much attention and significant advances have been made. Chapters in Section A dedicated to the cellular and molecular interactions between viruses and their hosts, exploring hosts cellular machinery for successful replication and movement and host defences that suppress infection. Section B discusses how these viruses evolve and invade new crops through recombination, reassortment, and mutation. This book also shows the most recent advances in RNA silencing and anti-viral defence, miRNAs in virus infection, transgenic and natural host resistances. There are important chapters that highlight Potyviridae, Geminiviridae, and Bromoviridae, which threaten global food security and agriculture sustainability. Section C is on Plant Virus Management, which provides knowledge generated at the molecular and cellular level that is being harnessed to deploy new strategies to limit virus infection in agricultural crops. This section includes chapters describing the implementation of small RNA technology, gene-editing technology, and natural resistance to control disease.

This book brings the information together in all aspects of plant viruses their evolution, host interaction and management. The range of topics will certainly satisfy the needs for general interest in a plant virus. Prof. Gaur, Prof. Khurana, Dr. Sharma and Prof. Hohn are very well-known plant virologist and has significant credentials in the field of Plant Virology and contributed other significant books highlighting critical advances in the field of Plant Virology. It is thrilling to see them take on this project and important topic. I think all who read this book will find this new edition, balancing the latest advances in the field dealing with modern approaches for crop and plant protection.

Preface of the first edition

Plant viruses have evolved as combinations of genes whose products interact with cellular components to produce progeny virus throughout the plant. Some viral genes, particularly those involved in replication and assembly, tend to be relatively conserved, whereas other genes that have evolved for interaction with a specific host, for movement, and to counter host-defense systems, tend to be less conserved.

The ability of the virus to move from the initially infected cell throughout the plant appears to be one of the major selective forces for the evolution of plant viruses. Successful systemic infection of plant viruses results from replication in initially infected cells, followed by two distinct processes: cell-to-cell and long-distance movement. Cell-to-cell movement is a process that allows the virus to pass to adjacent cells by successful interactions between virus-encoded movement proteins and host factors. Long-distance movement is a multistep process that allows the virus to enter the sieve element from an adjacent cell, followed by passive movement of the virus through the phloem to a distal region of the plant by exiting into a cell adjacent to the phloem. Further cell-to-cell movement from the phloem-associated cells allows the virus to invade most of the cells at a distal region of the plant. Viral proteins, and host factors that are involved in the cell-to-cell movement of plant viruses, have been widely examined. However, the host factors that are involved in long-distance transport of plant viruses and the mechanisms of long-distance movement—such as factors that are involved in virus entry into phloem tissue and virus exit at a distal region of the plant—are less well understood. Additionally, plants have host-defense mechanisms, including RNA silencing that must be overcome by the virus for effective movement within the plant. Viruses have evolved gene products to suppress these defense mechanisms.

The long-term research of the group focuses on understanding the emergence of new viral diseases. Plant viral diseases have a high socioeconomic impact, as they affect crop and forest productivity as well as ecosystem composition and dynamics. The highest impact of diseases in host populations is often caused by emerging diseases, defined as those whose incidence in a host population is increasing as a result of long-term changes in their underlying epidemiology. Major factors favoring disease emergence are genetic change in pathogen and host populations and changes in host ecology and environment. Hence, we proposed an edited book covering the research interests of the virus group and organized the chapters in and around plant virus evolution and the mechanisms of plant-virus interaction at a molecular level.

Editors

Preface of the second edition

Plant Virus-Host Interaction, edited by R.K. Gaur, S M Paul Khurana, Pradeep Sharma, and Thomas Hohn, is a comprehensive book on plant viruses and their interactions with host. It not only includes information related to plant viruses, but also provides cutting-edge research and emerging topics covered by plant virologists. Plant viruses are highly prevalent worldwide and one of the main threats to crops. For sustainable and healthy agricultural production, strategies for virus disease management must be developed and for these strategies to be effective, we require in-depth knowledge of the close interactions that viruses establish with the hosts.

After the great success of its first edition, this book provides an excellent update of the current knowledge on plant viruses and their management. We have included chapters on plant virus evolution and diversity, host interactions, and their management. The innovation in biological microscopy and in genome editing strategies have allowed virus researchers to explore connections between the virus and the host at subcellular levels, expand the capability to genetically probe the virus-host interactions, and identify novel antiviral targets.

The 22 chapters in this volume are divided into three sections, with the aim to present the recent progress on different aspects of plant virology. The chapters cover a variety of topics such as ecology and diversity, virus identification, virus-mediated modulation pathogenicity, and host defense.

Section A: Plant virus-host interaction

Section B: Plant virus evolution and diversity

Section C: Plant virus management

The research developments over the past decade have necessitated revising the edition to include a few important themes to retain material from the first edition, providing the basis for understanding newly recognized mechanisms. We hope to have expressed the enthusiasm of the subject and future directions that may prove to be scientifically useful. Overall, these works contain rich novel information from diverse viruses and interesting biological findings that warrant further detailed studies.

Plant virus research will contribute to further advance of virology in general as well as lay a solid foundation for research development of control methods of many virus diseases.

Lastly, the editors of this volume greatly appreciate contributions from all the authors and reviewers for their help to the collection.

Editors

Section A

Plant virus-host interaction

Chapter 1: Host-encoded miRNAs in plant-virus interactions—What's new

Zhimin Yin    Plant Breeding and Acclimatization Institute—National Research Institute, Młochów Research Center, Młochów, Poland

Abstract

In the last decade, especially by using the high-throughput small RNA (sRNA) or degradome next-generation sequencing (NGS), genome-wide miRNA and/or the cleaved mRNA target profiles responded to infection by viral pathogens were identified in different plant species. Moreover, the functions of individual miRNAs in plant-virus interaction were demonstrated, for example, by using reverse genetics approaches. This chapter documents the state-of-art list of virus-responsive host-encoded miRNAs and their mRNA targets, which covers 29 plant species and 12 DNA and 38 RNA virus species and highlights (1) miRNAs in pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI); (2) miRNAs in effector-triggered immunity (ETI); (3) miRNAs in host susceptibility; (4) symptom-related miRNAs; (5) cultivar-specific miRNAs; (6) miRNAs in transgenic virus resistant plants; (7) plant miRNAs directly targeting the virus genome for cleavage; and (8) multiple novel regulatory layers of miRNAs.

Keywords

miRNA; Plant; Virus; PTI; ETI; Susceptibility; phasiRNA; ta-siRNA; lncRNA; eTM

1: Introduction

Plant microRNAs (miRNAs) are endogenous noncoding RNAs of 20–24 nucleotides (nt) in length that regulate eukaryotic gene expression post-transcriptionally by targeting specific messenger RNAs (mRNAs) for cleavage or translational inhibition (Bartel, 2004; Chen, 2010; Voinnet, 2009), or transcriptionally by directing DNA methylation in some cases (Hu et al., 2014; Wu et al., 2010). In plants, miRNA genes (MIRs) are transcribed to primary miRNAs (pri-miRNAs) in nucleus by RNA polymerase II; the pri-miRNAs are processed by RNAse III-LIKE DICER-LICKE I ENDONUCLEASE (DCL1) to generate miRNA precursors (pre-miRNAs) (Kurihara and Watanabe, 2004; Papp et al., 2003). Further cleavage of the pre-miRNA by DCL1, HYPONASTIC LEAVES1 (HYL1) and SERRATE (SE) releases a miRNA/miRNA* duplex. The mature miRNA is selectively loaded into ARGONAUTE 1 (AGO1) and exported to the cytoplasm as an AGO1/microRNA complex by CHROMOSOMAL REGION MAINTENANCE1 (CMR1/EXPORTIN1) (Bologna et al., 2018); while the miRNA/miRNA* duplex is exported from the nucleus by HASTY (Park et al., 2005). In the cytosol, AGO1 loaded with miRNA is part of the RNA-induced silencing complex (RISC) and miRNA binds to mRNA and inhibits gene expression post-transcriptionally through perfect or near-perfect complementarity between the miRNA and the mRNA (Bartel, 2004).

Plant miRNAs play essential roles in plant development and their own biogenesis as well as in plant's response to biotic and abiotic stresses, virus infection included (Islam et al., 2018b; Jones-Rhoades et al., 2006; Khraiwesh et al., 2012; Liu et al., 2017b; Zhang et al., 2019a). Previously, a common set of miRNAs that responded to virus infection in a plant- and virus-independent manner, including miR168 and those development-related or stress-responsive ones, were summarized (Yin et al., 2014). However, many miRNAs and their targets respond to viral infection in a virus-, strain-, plant- and tissue-specific manner. The levels of miRNAs and their mRNA targets were altered antagonistically or up-regulated in parallel. In addition, novel miRNAs were identified in virus-infected plants.

Moreover, plant miRNAs play important roles in plant immunity (Islam et al., 2018a; Padmanabhan et al., 2009; Seo et al., 2013). The zigzag model for plant immunity was originally illustrated based on antibacterial/antifungal immune system (Jones and Dangl, 2006). In the modified zigzag model of virus-host interactions, viruses produce double-stranded RNA (dsRNA), which acts as a pathogen-associated molecular pattern (PAMP) in the infected plants and activates RNA silencing as a PAMP-triggered immunity (PTI)-like phase to target the viral RNAs (Moffett, 2009; Zvereva and Pooggin, 2012; Nakahara and Masuta, 2014). As a counterdefense, the viruses produce RNA silencing suppressors (RSSs) as viral effectors to suppress RNA silencing, resulting in effector-triggered susceptibility (ETS)-like phase. To counter counterdefense, plants coevolve and activate a resistance (R) gene-encoded protein that specifically recognizes a viral RSS as the avirulence (Avr) protein, leading to the effector-triggered immunity (ETI)-like phase. The viral Avr proteins are also virulence factors, which may suppress innate immune responses in the susceptible hosts, and are recognized by R proteins in the resistant hosts (Soosaar et al., 2005; Moffett, 2009; Zvereva and Pooggin, 2012). Plant miRNAs may participate in both PTI and ETI by regulation of key component in the antiviral RNA-silencing pathway or plant R genes (Wang et al., 2016, 2018b; Li et al., 2012; Shivaprasad et al., 2012).

In the last decade, especially by using high-throughput small RNA (sRNA) or degradome next-generation sequencing (NGS), genome-wide miRNA and/or the cleaved mRNA target profiles responded to infection by viral pathogens were identified in different plant species. The functions of individual miRNAs in plant-virus interaction were demonstrated, for example, by using reverse genetics approaches. This chapter documents the state-of-art list of virus-responsive host-encoded miRNAs and their mRNA targets, which covers 29 plant species and 12 DNA and 38 RNA virus species (Table 1) and highlights (1) miRNAs in PTI; (2) miRNAs in ETI; (3) miRNAs in host susceptibility; (4) symptom-related miRNAs; (5) miRNAs in synergism; (6) cultivar-specific miRNAs; (7) miRNAs in transgenic virus resistant plants; (8) plant miRNAs directly targeting the virus genome for cleavage; and (9) multiple novel regulatory layers of miRNAs.

Table 1

AGO, agronaute; AO, l-ascorbate oxidase; BraTNL1, a TIR-NB-LRR class of R gene; DCL, RNAse III-like DICER-like endonuclease; DEMs: differentially expressed miRNAs; DEGs, differentially expression genes (transcripts); eIFiso4G, the large scaffold protein isoform of the eukaryotic translation Initiation Factor 4F complex isoform (eIFiso4F); eTMs, endogenous target mimics; HD-Zip, HD-Zip transcription factor; miRNA, microRNA; miRNA*, antisense miRNA; ihpRNA, engineered inverted repeat construct. ihpRNA strategy; isomiR, miRNA length variant; MYB, MYB domain protein; NB-LRR, nucleotide binding site-leucine rich repeat; TIR-NB-LRR, NB-LRR protein with N terminal domain TIR; NbAGO1–1H and NbAGO1–1L, two homeologs of the AGO1-like gene in Nicotiana benthamiana; ORFs, open reading frames; OsMADS, rice MADS box protein; OsRDR1, rice RNA-dependent RNA polymerase 1; phasiRNAs, phased secondary small interfering RNAs; PHAS, phasiRNA-producing loci; RSV-NS3, rice stripe virus (RSV)-encoded nonstructural protein 3; SCL6, scarecrow-like 6; siRNAs, small interfering RNAs; SPL, squamosa promoter binding protein-like; TCP, TEOSINTE BRANCHED/CYCLOIDEA/PCF.

Refs: 1 (Du et al., 2014); 2 (Hu et al., 2011); 3 (Hajdarpašić and Ruggenthaler, 2012); 4 (Zavallo et al., 2015); 5 (Tagami et al., 2007); 6 (Wu et al., 2016); 7 (Liu et al., 2017a); 8 (Kundu et al., 2017); 9 (Cui et al., 2020); 10 (He et al., 2008); 11 (Wang et al., 2015b); 12 (Patwa et al., 2019); 13 (Akmal et al., 2017); 14 (Silva et al., 2011); 15 (Romanel et al., 2012); 16 (Permar et al., 2014); 17 (Liu et al., 2015a); 18 (Liang et al., 2019); 19 (Visser et al., 2017); 20 (Alabi et al., 2012); 21 (Bester et al., 2017a); 22 (Bester et al., 2017b); 23 (Pantaleo et al., 2016); 24 (Singh et al., 2012); 25 (Rubio et al., 2019); 26 (Gao et al., 2012); 27 (Xia et al., 2019); 28 (Zhou et al., 2016); 29 (Li et al., 2018); 30 (Xia et al., 2018); 31 (Gonzalez-Ibeas et al., 2011); 32 (Amin et al., 2011); 33 (Gursinsky et al., 2015); 34 (Du et al., 2019); 35 (Yin et al., 2015); 36 (Guo et al., 2017a); 37 (Diao et al., 2019); 38 (Xiao et al., 2014); 39 (Pacheco et al., 2012); 40 (Wang et al., 2018a); 41 (Abreu et al., 2014); 42 (Aryal et al., 2012); 43 (Zhang et al., 2019d); 44 (Liu et al., 2015b); 45 (Li et al., 2017); 46 (Yin et al., 2017); 47 (Križnik et al., 2017); 48 (Szajko et al., 2019); 49 (Sun et al., 2015); 50 (Zhang et al., 2019c); 51 (Du et al., 2011); 52 (Zhang et al., 2016a); 53 (Zhang et al., 2016b); 54 (Guo et al., 2012); 55 (Lian et al., 2016); 56 (Yang et al., 2016); 57 (Guo et al., 2015); 58 (Zheng et al., 2017); 59 (Wu et al., 2015); 60 (Wang et al., 2016); 61 (Tong et al., 2017); 62 (Yao et al., 2019); 63 (Zarreen et al., 2018); 64 (Xu et al., 2014); 65 (Ramesh et al., 2017); 66–68 (Chen et al., 2015, 2016, 2017a); 69 (Bao et al., 2018); 70 (Yin et al., 2013); 71 (Shiboleth et al., 2007); 72 (Reyes et al., 2016); 73 (Marmisolle et al., 2020); 74 (Lang et al., 2011a); 75 and 76 (Bazzini et al., 2007, 2011); 77 (Li et al., 2012); 78 (Deng et al., 2018a); 79 (Guo et al., 2017b); 80 (Yin et al., 2019); 81 (Cillo et al., 2009); 82–86 (Feng et al., 2009, 2011, 2012, 2013, 2014); 87 (Lang et al., 2011b); 88 (Shivaprasad et al., 2012); 89 (Chen et al., 2012); 90 (Wang et al., 2018c); 91 (Prigigallo et al., 2019); 92 (Tousi et al., 2017); 93 (Tripathi et al., 2018); 94 (Naqvi et al., 2010); 95 (Pradhan et al., 2015); 96 (Singh et al., 2016); 97 (Jodder et al., 2018); 98 (Wang et al., 2018b); 99 (Wang et al., 2015a); 100 (Chiumenti et al., 2018); 101 (Sun et al., 2017).

aDNA viruses: BadnavirusGVCV, grapevine vein clearing virus; BegomovirusACMV, African cassava mosaic virus; CbLCuV, cabbage leaf curl virus; CLCuMV/CLCuMB, cotton leaf curl Multan virus/cotton leaf curl Multan betasatellite (CLCuMB, a newly-established family Tolecusatellitidae, genus Betasatellite); TbCSV/TbCSB, tobacco curly shoot virus/tobacco curly shoot betasatellite; ToLCV, tomato leaf curl virus; ToLCNDV, tomato leaf curl New Delhi virus; TYLCV, tomato yellow leaf curl virus; TYLCCNV/TYLCCNB, tomato yellow leaf curl China virus/tomato yellow leaf curl China betasatellite; TYLCSV, tomato yellow leaf curl Sardinia virus; MYMIV, mungbean yellow mosaic India virus; Tungrovirus RTBV, rice tungro bacilliform virus. RNA viruses: Ampelovirus GLRaV-3, grapevine leafroll-associated virus 3; Benyvirus BNYVV, beet necrotic yellow vein virus; CapillovirusASGV, apple stem grooving virus; Carmovirus HCRSV, hibiscus chlorotic ringspot virus; MNSV, melon necrotic spot virus; TCV, turnip crinkle virus; Cucumovirus CMV, cucumber mosaic virus; TAV, tomato aspermy virus; Fijivirus RBSDV, rice black streaked dwarf virus; SRBSDV, southern rice black-streaked dwarf virus; Foveavirus ASPV, apple stem pitting virus; GRSPaV, grapevine rupestris stem pitting-associated virus; Machlomovirus MCMV, maize chlorotic mottle virus; Ophiovirus CPsV, citrus psorosis virus; Oryzavirus RRSV, rice ragged stunt virus; Phytoreovirus RDV, rice dwarf virus; Polerovirus CLRDV, cotton leafroll dwarf virus; Potexvirus PVX, potato virus X; Potyvirus PPV, plum pox virus; PRSV, papaya ringspot virus; PVA, potato virus A; PVY: potato virus Y; SCMV, sugarcane mosaic virus; SMV, soybean mosaic virus; TEV, tobacco etch virus; TuMV, turnip mosaic virus; WMV, watermelon mosaic virus; ZYMV, zucchini yellow mosaic virus; Tenuivirus RSV, rice stripe virus; Tobamovirus CGMMV, cucumber green mottle mosaic virus; ORMV, oilseed rape mosaic virus; TMV, tobacco mosaic virus; ToMV, tomato mosaic virus; TobravirusTRV, tobacco rattle virus; Tombusvirus CymRSV, cymbidium ringspot virus; Tospovirus GBNV, groundnut bud necrosis virus; Waikavirus RTSV, rice tungro spherical virus; PMeV, papaya meleira virus, unassigned virus, similar to mycoviruses tentatively classified in the family Totiviridae.

2: miRNAs in PTI—Antiviral RNA-silencing pathway

The antiviral RNA silencing pathway, which constitutes the PTI-phase in plant antiviral immunity, directly targets viral RNAs; and is induced by viral dsRNA molecules (Ding and Voinnet, 2007). These viral dsRNAs are recognized by the plant and are processed into the primary virus-derived small interfering RNAs (vsiRNAs) of 21-nt by DCL4 and of 22-nt by DCL2 (Deleris et al., 2006; Llave, 2010; Qu et al., 2008; Waterhouse and Fusaro, 2006). The secondary vsiRNAs are produced from the aberrant viral transcription byproducts, which are generated by the primary vsiRNAs (Garcia-Ruiz et al. 2010; Wang et al., 2010b). Both the plant RNA-DEPENDENT RNA POLYMERASE1 (RDR1) and RDR6 contribute in the biogenesis of vsiRNAs (Qi et al., 2009). The vsiRNA is incorporated into AGO1-, AGO2-, or AGO7-containing RISC and degrades the viral RNA with sequence complementary to it (Alvarado and Scholthof, 2012; Bortolamiol et al., 2007; Harvey et al., 2011; Takeda et al., 2008; Wang et al., 2012).

MiR444 is a monocot-specific miRNA. In rice (Oryza sativa), miR444 and its MADS box targets directly control the transcription of OsRDR1, a key component of the antiviral RNA-silencing pathway (Wang et al., 2016). Without virus infection, the miR444 targets, the MIKCC-type MADS box proteins OsMADS23, OsMADS27a, and OsMADS57, form homodimers and heterodimers between them to repress the expression of OsRDR1 by binding to the CArG motifs of its promoter. Upon rice stripe virus (RSV) infection, the levels of miR444 increased, which diminishes the repressive roles of its targets MADS box proteins on OsRDR1 transcription, thus activating the OsRDR1-dependent antiviral RNA-silencing pathway. Overexpression of miR444 improves rice resistance against RSV infection accompanied by the up-regulation of OsRDR1 expression. However, reduced OsRDR1 expression by overexpression of miR444-resistant OsMADS57, or knockout of OsRDR1, reduced rice resistance against RSV (Wang et al., 2016). Alternatively, the miR444-regulated nitrate signaling may play roles in subsidizing the rice antiviral response, by manipulating the nitrogen status during virus infection (Yan et al., 2014).

3: miRNAs in ETI

Several classes of miRNAs, e.g., miR482, miR1885, miR6019, miR6020, miR6022 and miR6027, among others, have been proven to play key roles in ETI by regulation of R genes (Cui et al., 2020; Deng et al., 2018a; Križnik et al., 2017; Li et al., 2012, 2017; Prigigallo et al., 2019; Shivaprasad et al., 2012; Wang et al., 2018b).

The activity of resistance proteins (R proteins), which are encoded by R genes, must be strictly controlled to prevent autoimmunity, in which an immune response is activated in the absence of invading pathogens and causes deleterious effects on plant growth (Oldroyd and Staskawicz, 1998; Stokes et al., 2002). The majority of R proteins are the nucleotide binding site-leucine-rich repeat (NB-LRR or NLR)-containing proteins, which are further classified into coiled-coil (CC)-NB-LRR (CNL) or Toll/interleukin 1 receptor-like (TIR)-NB-LRR (TNL) protein families based on their variable N-terminal domain (Bonardi et al., 2012; Dangl and Jones, 2001).

The miRNAs of 22-nt in length, including the NLR-targeting miRNAs, a size that can trigger the biogenesis of secondary small interfering RNA (siRNAs) in a phased pattern relative to the miRNA cleavage site; these small RNAs are termed phasiRNAs (Chen et al., 2010; Cuperus et al., 2010; Deng et al., 2018b; Fei et al., 2013, 2016; Richard et al. 2018; Seo et al., 2018). The phasiRNAs may regulate their own targets in cis or other members of the target gene family in trans (Fei et al., 2013, 2016). Furthermore, when a noncoding transcript is sliced by a miRNA, it generates a subset of phasiRNAs known as trans-acting siRNAs (ta-siRNAs); the ta-siRNAs function outside of the local region and regulate the target protein-coding genes via mRNA cleavage in trans (Allen et al., 2005; Fei et al., 2013). The phasiRNA-producing loci (PHAS loci) could be protein-coding or non-coding genes; while the ta-siRNA-generating loci (TAS) are non-coding genes (Allen et al., 2005; Vazquez et al., 2004). The generated phasiRNAs are incorporated into the AGO proteins that induce target mRNA cleavage. The phasiRNAs might act synergistically with the miRNA triggers, leading to enhanced and amplified regulation of NLR transcripts and minimizing the overall metabolic cost for producing R proteins (Richard et al., 2018; Shivaprasad et al., 2012); they add zing to the zigzag model of plant defense (Fei et al., 2016).

Cui et al. (2020) demonstrated that a 22-nt miRNA in Brassica, miR1885, regulates both an R gene and a development-related gene through direct and trans-acting RNA silencing, respectively. The Brassica miR1885 targets both the TIR-NB-LRR class of R gene BraTNL1, and the TIR domain-containing gene BraTIR1, which lacks the NB-LRR domain. BraTIR1 functions as a TAS gene in the production of ta-siRNAs to silence the Brassica chlorophyll protein 24-encoding gene (CP24), BraCP24, which supposed to be involved in light harvesting and photosynthesis regulation (de Bianchi et al., 2008; Kovacs et al., 2006). Without pathogen attack, miR1885 was kept at low levels to maintain normal development and basal immunity but peaked during the floral transition to promote flowering. Upon turnip mosaic virus (TuMV) infection, miR1885-dependent trans-acting silencing of BraCP24 was enhanced to speed up the floral transition, whereas miR1885-mediated R gene turnover was overcome by TuMV-induced BraTNL1 expression (Cui et al., 2020).

Li et al. (2012) identified two tobacco miRNAs, the 22-nt miR6019 and the 21-nt miR6020, that guide cleavage of transcripts of the TNL-type tobacco mosaic virus (TMV) resistance N gene, and coexpression of N with miR6019 and miR6020 resulted in attenuation of N-mediated resistance to TMV. The N gene regulation is accompanied by the production of miR6019-triggered N-derived phasiRNAs (Deng et al., 2018a; Li et al., 2012). Deng et al. (2018a) further demonstrated the role of tobacco miR6019 and miR6020 in regulation of N gene during plant growth. The levels of N transcripts increased gradually during plant growth. The growth regulation of N expression was post-transcriptionally mediated by MIR6019/6020 whereas MIR6019/6020 was regulated at the transcriptional level during plant growth. The N-mediated immunity, as studied by using an N-miR6019/6020-TMV trilateral system, enhanced as plants matured, which correlated well with the increased accumulation of N transcripts.

The miR482 and miR2118 superfamily is abundance in different plant species and the members of this family target P-loop motif of the NB-LRR genes for the mRNA cleavage and are the triggers for producing phasiRNAs from their NB-LRR targets (Shivaprasad et al., 2012). The tomato miR482 directed the cleavage of mRNA of a CC-NB-LRR type protein, which defined the first position in the phased registers, and initiated production of phasiRNAs (Shivaprasad et al., 2012). In virus-infected plants, the miR482-mediated silencing cascade is suppressed, resulting in the enhanced expression of the NB-LRR mRNAs. This virus-inducible expression of R gene is most likely due to the action