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Delayed Maize Lateral Root Determinacy Induced by Mild Water Deficit

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Delayed Maize Lateral Root Determinacy Induced by Mild Water Deficit DELAYED MAIZE LATERAL ROOT DETERMINACY INDUCED BY MILD WATER DEFICIT _______________________________________________________ A Dissertation Presented to the Faculty of the Graduate School at the University of Missouri-Columbia _______________________________________________________ In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy _____________________________________________________ by TYLER G. DOWD Dr. Robert E. Sharp and Dr. David M. Braun, Dissertation Co-supervisors JULY 2017 The undersigned, appointed by the dean of the Graduate School, have examined the dissertation entitled DELAYED MAIZE LATERAL ROOT DETERMINACY INDUCED BY MILD WATER DEFICIT Presented by Tyler G. Dowd A candidate for the degree of Doctor of Philosophy And hereby certify that, in their opinion, it is worthy of acceptance. Dr. Robert E. Sharp Dr. David M. Braun Dr. Felix B. Fritschi Dr. Mel J. Oliver DEDICATION This dissertation is dedicated to my mother Linda Dowd for all her unwavering support, love and enthusiasm for everything I do. This would not have been possible without her guidance and good grace. Thank you. ACKNOWLEDGEMENTS First, I would like to express my deepest gratitude to my co-advisors, Dr. Robert E. Sharp and Dr. David M. Braun, whose excellent mentorship and dedication to research has motivated and encouraged me throughout my Ph.D. program. Without their guidance and assistance during challenging times, regarding both my research as well as personal struggles, this dissertation would not have been possible. Furthermore, I would also like to thank my committee members Dr. Felix B. Fritschi and Dr. Mel J. Oliver for their insight and assistance in improving my project and discussing difficulties as they arose. I would also like to thank my lab members who helped me when I was starting out my Ph. D. and welcomed me to the University of Missouri, Dr. Kara Riggs, Hallie Thompson, Dante Smith, Dr. Priya Voothuluru, Dr. Kristen Leach, Dr. Saadia Bihmidine and Erin Finefield. To all my friends in Columbia, I would like to thank you for all of the wonderful times spent together during my studies. Dr. Morgan Halane, Sam McInturf, Robert Mecchi, Dr. Morgan McCaw, Shawn Abrahams, Dr. Chris Garner, Sarah Unrah, Dr. Michael Gardner, and Ben Spears. You will all be missed and I hope the time before seeing you again will be brief and full of happiness. Of particular importance, I would like to give my unending thanks to my wife Carola De La Torre Dowd, who always stood by me regardless of circumstance or the difficulty of any situation. And to our son Dominik Liam Dowd, who can always cheer me up and pull me away from any drama or hardship. The two of you have ii made the world greater and made me who I am. I certainly cloud not have accomplished this without their daily presence and inspiration. Finally, I would like to thank my parents, Linda Dowd, Dave Dowd and Gina Dowd for believing in me and supporting the choices I have made in life with wide arms, open minds and loving hearts. Thank you, for everything. iii TABLE OF CONTENTS ACKNOWLEDGEMENTS ……………………………………..……………… ii LIST OF TABLES ……………………………………………………….……… x LIST OF FIGURES …………………………………………………….……….. x ABSTRACT ……………………………………………………………………… xiii CHAPTERS 1. LITERATURE REVIEW Introduction …………………………..………………………………………… 2 Maize root system morphology and the role of lateral roots………….…….. 3 Lateral root responses to water deficit……………………………..………..... 5 Root cellular plasticity responses to water deficit.……….…………….…….. 6 Lateral root development……….………………………………………………. 7 Root meristem organization and maintenance……………………………….. 19 Determinate root growth.………………………………………………..……... 23 iv Objectives…………………………………………………………….…………. 27 References.…………………………………………………..……………….… 28 2. MAIZE LATERAL ROOT DEVELOPMENTAL PLASTICITY INDUCED BY MILD WATER STRESS I: AN EXAMINATION OF GENOTYPIC VARIATION ACROSS A HIGH-RESOLUTION SERIES OF WATER POTENTIALS Abstract …………………………..……………………………..…………..….. 38 Introduction …………………………..……………………………..……..…… 39 Materials and Methods ………………………….…………………..…….….. 43 Growth media water relations ……………………………………………….… 43 Plant material and growth conditions ………………………………….……… 44 Root trait analysis from scans …………………………………………………. 45 Statistical analysis ………………………………………………………………. 46 Results ………………..………………………………………………………… 47 Comparative water relations of common plant growth media ……………… 47 A near-stable water deficit environment for the comparison of root traits ……………………………….……………………………………... 55 Maize axial root responses to mild water deficit conditions ….…………….. 57 v FR697 displays enhanced lateral rooting under mild wild water deficit conditions …………………………………………...……………...……. 57 First-order lateral root plasticity ……………………………………………….. 65 Dry-matter accumulation ………………………………………………………. 71 Discussion………………………………………………………………………. 73 Suitability of various growth media for sustained mild water deficit experiments ……………………………………………………………… 73 Genotypic differences in maize lateral root plasticity induced by mild water deficit …….………………………………..…………………..… 77 An interaction between lateral root plasticity and determinate growth? ………………………………………………….…………………..…… 81 References………………………………………………………………………. 83 3. MAIZE LATERAL ROOT DEVELOPMENTAL PLASTICITY INDUCED BY MILD WATER STRESS II: GENOTYPE SPECIFIC SPATIO-TEMPORAL EFFECTS ON DETERMINATE DEVELOPMENT Abstract ………………………………………………………………………… 89 Introduction ……………………………………………………………………. 91 Materials and Methods ………………………………………………………. 93 Plant growth conditions ………………………………………………………… 93 vi Root trait analysis from scans …………………………………………………. 95 Optical clearing of first-order lateral roots ……………………………………. 96 Analysis of cell length profiles …………………………………………………. 96 Kinematic equations from anatomical records ………………………………. 97 Longitudinal, radial plus tangential, and volumetric strain rates ……………. 98 Statistical analysis ………………………………………………………………. 99 Results……………….…………………………………………………………... 99 Stability of media water status for assessment of lateral root development …………………………………………………………………….. 99 Whole root system responses to mild water deficit ……………………….… 100 First-order lateral root length, elongation and acceleration influenced by mild water deficit ………………………………………………... 104 Effects of mild water deficit on first-order lateral root diameter and volume changes associated with determinate growth ...……………….. 107 Anatomical modifications of determinate growth influenced by mild water deficit ………………………………………………………………… 109 Cell flux patterns associated with determinate growth are affected by mild water deficit ………………………………………...…………………... 111 Spatio-temporal distribution of longitudinal expansion influenced by determinacy and mild water deficit ………………………………...………. 114 vii Spatio-temporal distribution of cross-sectional area expansion influenced by determinacy and mild water deficit ……………………………. 119 Spatio-temporal distribution of volumetric expansion influenced by determinacy and mild water deficit ……………………………..…………. 123 Discussion …………………………………………………………………...... 125 Genotype-specific whole root system responses to mild water stress ……. 125 Genotypic differences in well-watered first-order lateral root growth and development ……………….……………………………….………………. 127 Delayed determinate growth of FR697 first-order lateral roots induced by mild water deficit conditions ……………………….……………………….. 131 Possible mechanisms of interaction between mild water deficit and determinate growth control …………………………………………………….. 135 Conclusions…………………………………………………………………….. 138 References………………………………………………………………………. 138 4. SUMMARY AND FUTURE DIRECTIONS Summary ………………………………………………………………………... 146 Potential benefits of delayed determinate growth in water-limited conditions ………………………………………………………………………… 147 viii Radial anatomical modifications induced by mild water deficit and the consequences on lateral root mechanical strength …………………………. 148 Spatio-temporal analysis of the genetic control of delayed lateral root determinacy induced by mild water deficit …………………………………… 152 Genotypic variation in hydrotropism and hydropatterning …………………. 154 Real-time observations of alterations in growth and resource allocation of mild water deficit induced delayed determinacy ………………………….. 155 Alternative growth conditions ………………………………………………….. 156 Extension of findings to older plants, different root systems and other species …………………….………………………………………… 158 References…….………………………………………………………………... 160 APPENDIX ………………………………………………………………………... 166 Non-transpiring system comparison of lateral root responses to decreasing growth medium water potential ……………………..…………… 166 Ineffectiveness of Greens Grade and sand to maintain a stable water potential …………………………………………………….…………….. 168 Water deficit-induced lateral root plasticity of Mo17 ..……………………….. 169 Enhancement of FR697 lateral root length in response to mild water deficit in other growth media ………………………………..………….. 170 ix VITA………………………………………………………………………………. 171 LIST OF TABLES Tables Page 2-1 Validation of stable media Ψw across a gradient of mild water deficits…………………………………………..………… 56 3-1 Media Ψw was stable throughout lateral root development… 101 LIST OF FIGURES Figures Page 1-1 The categories of roots in Zea mays and their origin ………. 4 1-2 Morphological stages of lateral root development …………… 11 1-3 Auxin-dependent processes facilitating cell separation and LRP emergence ……………………………….. 16 1-4 Anatomical organization of the root apical meristem …...…… 21 2-1 Influence of gravimetric water content on the water potential of several
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