Crop Science
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Published online 20 May 2008
Published in Crop Sci 48:992-999 (2008)
© 2008 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF) Free
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Basso, C. F.
Right arrow Articles by Tracy, W. F.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Basso, C. F.
Right arrow Articles by Tracy, W. F.
Agricola
Right arrow Articles by Basso, C. F.
Right arrow Articles by Tracy, W. F.
Related Collections
Right arrow Crop Growth and Development
Right arrow Crop Genetics

Divergent Selection for Vegetative Phase Change in Maize and Indirect Effects on Response to Puccinia sorghi

C. F. Basso, M. M. Hurkman, E. S. Riedeman and W. F. Tracy*

Dep. of Agronomy, College of Agricultural and Life Sciences, Univ. of Wisconsin–Madison, Madison, WI 53706. Contribution from the Wisconsin Agric. Exp. Sta. Research supported by Hatch funds and the College of Agric. and Life Sciences, Univ. of Wisconsin-Madison

* Corresponding author (wftracy{at}wisc.edu).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
In maize (Zea mays L.), some experiments have indicated that early vegetative phase transition is associated with increased resistance to disease, insects, and stalk lodging. The sweet corn population Minn11 was selected over three cycles of divergent recurrent selection for early-phase transition and late-phase transition. Objectives were to determine the effectiveness of divergent recurrent selection and if the divergent selection program was associated with resistance to common rust (Puccinia sorghi). Selection resulted in a significant linear response for last leaf with juvenile wax in both the early and late directions of selection. The third cycle in the late direction (C3L) had two more leaves with juvenile wax than cycle zero (C0). The third cycle in the early direction (C3E) had 1.5 fewer leaves with juvenile wax than C0. To determine the effects of divergent selection for vegetative phase change on response to common rust the populations were inoculated with rust at three developmental times, vegetative stage (v) 5, v10, and v15, and rust damage was rated on leaves 7 through 13 individually, resulting in 21 potential responses for each direction of selection. Among the 21 leaf by developmental stage combinations, there were 9 significant linear trends in the late direction of selection. Most of the linear trends were detected in leaves 7 through 9. Selection for early transition did not affect response to common rust. The amount of leaf area damaged by rust in C3E never differed from the amount in C0.

Abbreviations: C, Cycle • E, early • L, late


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
DURING DEVELOPMENT, higher plants progress through four distinct developmental phases: embryonic, juvenile vegetative, adult vegetative, and reproductive (Poethig, 1990). In maize (Zea mays), phase change from juvenile vegetative to adult vegetative occurs gradually, in a coordinated manner, at predictable times, and it involves subtle changes in shoot morphology and physiology. Transition from the adult vegetative phase to the reproductive phase involves extreme morphological changes as vegetative structures are either suppressed or modified to form inflorescences (Poethig, 1990).

Phase-specific morphological and physiological differences exist between upper and lower leaves in maize, and these differences have led to their classification into the different phases of vegetative growth, juvenile vegetative and adult vegetative (Poethig, 1990; Lawson and Poethig, 1995; Bongard-Pierce et al., 1996). Juvenile leaves are typically shorter and narrower than adult leaves, have a thin cuticle, lack bulliform cells and trichomes, and are covered with an epicuticular wax that is bluish-gray in appearance and, on wetting, causes water to bead. The epidermal cells of juvenile leaves stain purple with Toluidine Blue. In addition to being longer and wider than juvenile leaves, adult leaves are thicker, possess a thicker cuticle, have bulliform cells and three types of trichomes on the adaxial surface (macrohairs, bicellular, and prickle hairs), and have only cuticular wax, which gives the leaves a glossy green appearance and increased wettability (Bianchi and Marchesi, 1960; Avato et al., 1987). The epidermal cells of adult leaves stain aqua with Toluidine Blue. Juvenile and adult leaves also differ in cell wall composition (Bergvinson et al., 1995). Juvenile nodes produce adventitious roots and axillary buds that may develop into tillers (vegetative branches), while adult axillary buds either develop into ear primordia or are suppressed. Adult nodes do not produce adventitious roots (Poethig, 1990). Because they are readily observable features of the epidermis, first leaf with visible cuticular wax and presence of macrohairs on the leaf blade serve as markers to distinguish initiation of the adult vegetative phase of maize-shoot development (Lawson and Poethig, 1995). Last leaf with epicuticular wax, last node with adventitious roots, and tiller number are useful traits in distinguishing the duration of the juvenile vegetative phase (Abedon et al., 1996; Abedon, 1997), although the latter two traits are not as diagnostic as last leaf with epicuticular wax.

Maize genotypes generally express juvenile traits in the first five to six nodes. Beginning with the sixth or seventh node, juvenile traits are gradually replaced with adult traits, so that from the eighth node to the terminal inflorescence, only adult vegetative tissues are formed (Moose and Sisco, 1994). Leaves produced during the transition from juvenile to adult phase express traits characteristic of both juvenile and adult vegetative phases in different parts of the leaf. Studying a diallel among seven sweet corn populations, Abedon et al. (1996) found that last leaf with juvenile wax, last node with adventitious roots, and first leaf with adult wax visible were positively correlated, indicating that the time of the juvenile vegetative and adult vegetative phases were associated in these populations. Vegetative phase change from juvenile to adult is regulated independently from reproductive phase change (Poethig, 1988; Abedon, 1997).

Some studies have reported that the adult vegetative phase has increased resistance to stalk lodging and certain diseases and insects relative to the juvenile vegetative phase (Abedon et al., 1999; Leonard and Thompson, 1976; Headrick and Pataky, 1987; Bergvinson et al., 1995; Abedon and Tracy, 1996; Williams et al., 1998), as well as increased photosynthetic activity (Thiagarajah et al., 1981) and xeromorphism (Esau, 1977). Other studies have found no relationship between vegetative phase and pest resistance (Hurkman, 2002; Revilla et al., 2005a,b). Abedon and Tracy (1998), studying changes in phase change traits in three sweet corn populations selected for resistance to common rust (Puccinia sorghi), found that one of the three populations had a reduced juvenile phase. Phase change in the other two populations did not change in response to selection for rust resistance, indicating that a relationship between phase change and rust resistance exists in some but not all genetic backgrounds. Hurkman (2002) found that the relationship between resistance to common rust and timing of phase change was complicated by the developmental time the plants were inoculated with Puccinia sorghi.

One way to test the hypothesis that the timing of vegetative phase change has an affect on resistance to common rust is to develop populations divergent for phase change from a common genetic base. Revilla et al. (2002) demonstrated that divergent selection for phase change was effective in EPS5, a synthetic population from Spain. In Wisconsin the sweet corn population Minn11 has been selected for three cycles of divergent recurrent selection for last leaf with juvenile wax. A correlated response to selection for last leaf with juvenile wax in resistance to common rust would provide support for the hypothesis that timing of vegetative phase change is associated with resistance to common rust. Determining the response to common rust of individual leaves in the transition zone may clarify the relationships among rust resistance, phase change, and timing of inoculation. The objectives of this study were to determine (i) if divergent selection for timing of vegetative phase change was effective and (ii) if divergent selection for timing of vegetative phase change is associated with resistance to common rust in leaves in the transition zone.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Population Development
The sugary1 (su1) population Minn11, developed by Dr. D. Davis of the University of Minnesota, formed Cycle 0 (C0) of a recurrent selection program at the University of Wisconsin that consisted of three cycles of divergent recurrent selection for last leaf with juvenile wax. Minn11 was created by intermating sweet corn and field corn inbreds and selecting only su1 kernels from the subsequent progeny. In 1994 seed of C0 was planted, approximately 150 plants were self-pollinated, and the selfed ears harvested. Seed from the selfed ears were planted in family rows. The following year, families were evaluated for last leaf with juvenile wax. The earliest and latest 20% were selected. Within each direction of selection, selected families were intermated using pollen bulks from the selected families. A minimum of 100 plants in each population were used as females. Balanced bulks were made with seed from the resulting ears and this recombination step resulted in Cycle 1 early (C1E) and Cycle 1 late (C1L). Remnant seed from the ears was planted ear to row, and each row was considered a family for the next cycle of selection. The process was repeated in 1996 and 1997 for a total of three cycles of selection in the early and late directions.

Evaluation of Phase Change
Field trials were conducted at the West Madison Agricultural Experiment Station, Madison, WI, in a Plano silt loam (fine-silty, mixed, superactive, mesic Typic Argiudolls) in 1998, 1999, and 2000 and at the Arlington Agricultural Research Station, Arlington, WI, in a Plano silt loam in 2000. Cycles C0, ClE, C2E, C3E, C1L, C2L, and C3L were grown in randomized complete blocks with three replications per environment. Plantings were made at the West Madison Agricultural Experiment Station on 1 June 1998, 15 May 1999, and 15 May 2000 and at the Arlington Agricultural Research Station on 29 Apr. 2000. In 1998 four row plots were planted and data were taken from the center two rows. In 1999 and 2000, three row plots were planted and data were taken from the center row. Data were taken on six bordered plants per row. In 1998 the rows were 4.1 m long and 0.76 m apart with 25 kernels planted and subsequently thinned to 15 plants per row for a final density of 44,500 plants ha–1. In 1999 the rows were 3.5 m long and 0.76 m apart with 25 kernels planted and subsequently thinned to 12 plants per row for a final density of 41,500 plants ha–1. At the West Madison Agricultural Research Station in 2000, the rows were 3.5 m long and 0.76 m apart with 22 kernels planted and subsequently thinned to 15 plants per row for a final density of 50,000 plants ha–1. At the Arlington Agricultural Research Station in the same year, the rows were 7.6 m long and 0.76 m apart with 48 kernels planted and subsequently thinned to 32 plants per row for a final density of 50,000 plants ha–1.

Duration of the juvenile phase was determined visually by the last leaf with juvenile wax, and initiation of adult vegetative growth was determined as the first leaf with adult wax. To determine if variation in the timing of vegetative-phase change in this population affects leaf number, leaves below the ear and total leaf number were also scored. Last leaf with juvenile wax was evaluated in four environments, first leaf with adult wax in two environments, and the leaf number traits in three environments.

Data from individual plants were expressed on the basis of entry means for analysis of variance using SAS software (SAS Institute, 1994) using the mixed procedure. Cycle effects were considered fixed, and all other effects were considered random. Cycle effects were divided into two linear regression models that combined single degree of freedom orthogonal contrasts for the high and low directions of selection, as proposed by Eberhart (1964). If significant, a two quadratic regression model was also tested. To provide a statistic for comparing the direction and degree of response to divergent selection, significant two linear or two quadratic regression models were divided into average and among single degree of freedom orthogonal contrasts. A significant average contrast indicates that the response in one direction of selection was greater than in the other direction or responses occurred in the same direction. A significant among contrast indicates that responses to divergent selection differed. Least significant differences at p ≤ 0.05 were used to compare cycle means, averaged across years and replications. Pearson correlation coefficients were determined from data averaged over environments and blocks (n = 7).

Evaluation of Rust Resistance
Field trials were conducted at the West Madison Agricultural Research Station in a Plano silt loam in 2001 and 2002 and at the Arlington Agricultural Research Station in a Plano silt loam in 2002. Cycles C0, C1E, C2E, C3E, C1L, C2L, and C3L were grown in randomized complete blocks with three replications and three planting dates. Planting dates were spaced to have plants at time of rust inoculation at approximately vegetative stage 5 (v5), vegetative stage 10 (v10), and vegetative stage 15 (v15) (Ritchie et al., 1993).

The first plantings were made at the West Madison Agricultural Research Station on 15 May 2001 and 4 May 2002 and at the Arlington Agricultural Research Station on 7 May 2002. The second plantings were made at West Madison on 10 June 2001 and 7 June 2002 and at Arlington on 17 June 2002 as the plants from the first planting reached the v5 stage of development. The third plantings were made at West Madison on 20 June 2001 and 25 June 2002 and at Arlington on 26 June 2002 as the plants from the second planting reached the v5 development stage. Three row plots were planted by hand, and data were taken from the center row. Rows were 3.5 m long and 0.76 m apart with 20 kernels planted and subsequently thinned to 12 plants per row for a final density of 41,500 plants ha–1.

At the v4 stage of development of the last planting, during the second week in July, all plants in the experimental rows were inoculated with common rust by injecting 3 mL of an urediniospores suspension (5 mg of urediniospores in 400 mL H2O with 5 drops of Tween 20 added to prevent clumping) into the whorl using a backpack sprayer. The inoculum was provided by Dr. Jerald K. Pataky, University of Illinois. In addition, all plants were exposed to natural inoculum so the levels of infection were a combination of artificial and natural inoculum. The percentage of leaf area damaged by rust was determined by visual observation and rated from 0 to 100%. To evaluate individual leaves for percentage of leaf area damaged, it was necessary to mark a specific leaf on each of six plants in each family row as a point of reference. The eighth leaf of each of the six plants was clearly marked with a hole made by a paper punch. Due to natural senescence of leaves produced early in development, it was necessary to move the mark upward at later stages of development. Rust damage was evaluated at the end of anthesis. Six plants in each experimental row were visually evaluated on the basis of the percentage of leaf area damaged by rust. Individual leaves, from leaf number 7 to leaf 13, were evaluated.

Data from individual leaves were expressed on the basis of entry means for analysis of variance using SAS software (SAS Institute, 1994), using the mixed model procedure. Cycles of selection, leaf number, and developmental stage effects were considered fixed; all other effects were considered random. Least significant differences at p ≤ 0.05 were used to compare cycle means, averaged across environments and blocks. To calculate LSDs to compare means among different leaves at different developmental stages the mixed model procedure was used. Linear regression analysis was performed using SAS software (SAS Institute, 1994).


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Developmental Traits
Significant environment effects were observed for last leaf with juvenile wax and leaves below the ear (Table 1 ). Cycle effects were significant for last leaf with juvenile wax, first leaf with adult wax, leaves below the ear, and total leaf number. Only last leaf with juvenile wax had a significant cycle by environment interaction, which resulted from a change in magnitude of the response, not a change in rank. Two linear regressions were significant for last leaf with juvenile wax, first leaf with adult wax, leaves below the ear, and total leaf number (Table 1), indicating that all traits were affected by selection. Two quadratic regressions were also significant for first leaf with adult wax, leaves below the ear, and total leaf number. Coefficient of determination (R2) values for these traits ranged from 0.78 to 0.89 (Table 2 ).


View this table:
[in this window]
[in a new window]

  		Table 1. Mean squares from ANOVAs for phase-specific traits in Cycle zero (C0), cycles in late direction (L) C3L, C2L, C1L, and cycles in the early direction (E) C1E, C2E, and C3E of Minn11 sweet corn divergently selected for last leaf with juvenile wax.{dagger}

 

View this table:
[in this window]
[in a new window]

  		Table 2. Means and least squares estimates of indirect responses in phase-specific and agronomic traits for seven cycles of Minn11 sweet corn divergently selected for last leaf with juvenile wax, averaged across three environments.{dagger}

 
First leaf with adult wax had significant among linear and nonsignificant average linear contrasts (Table 1), indicating that responses to divergent recurrent selection were in opposite directions and approximately equal in magnitude (Table 2). Significant average and among contrasts (either linear or quadratic) occurred for last leaf with juvenile wax, leaves with rust, leaves below the ear, and total leaf number, indicating that the response in one direction of selection was significantly greater in magnitude or had a different trend than in the other direction. For both leaf number traits, there were no significant changes in the early direction of selection, while selection in the late direction significantly altered the number of leaves (Table 2). Averaged over environments, last leaf with juvenile wax and first leaf with adult wax increased in the late direction and decreased in the early direction of selection. C3L had two more leaves with juvenile wax than did C0. C3E had 1.5 fewer leaves with juvenile wax than C0.

Last leaf with juvenile wax was correlated with first leaf with adult wax (0.97, P < 0.01), leaves below the ear (0.92, P < 0.01), and total leaf number (0.98, P < 0.01) over cycles of selection. The direction and magnitude of responses was similar for total leaf number and leaves below the ear and resulted in a highly significant correlation (0.97, P < 0.01). First leaf with adult wax was highly correlated with leaves below the ear (0.95, P < 0.01) and with total leaf number (0.97, P < 0.01). These data support the concept of a coordinated reproductive developmental program whereby leaves below the ear and total leaf number tend to be highly conserved (Galinat, 1988) and that phase-specific traits can be positively correlated with leaves below the ear (Abedon, 1997; Poethig, 1988).

Rust Resistance
Percentage leaf area damaged by rust differed among environments, blocks, and cycles. Developmental stage and leaf number main effects did not affect percentage leaf area damaged by rust. However, numerous interactions significantly affected percentage leaf area damaged by rust: environment by developmental stage, environment by cycle, environment by leaf, environment by developmental stage by cycle, environment by developmental stage by leaf, and cycle by leaf. Developmental stage was not significant due to large environment by developmental stage interaction. In both 2002 environments, v5 developmental stage at time of inoculation had the greatest percentage leaf area damaged by rust, v15 had the least, and v10 was intermediate (Table 3 ). Juvenile or adult leaves that were new at the time of inoculation were more susceptible to rust than old juvenile or adult leaves. This may be because new leaves emerge from the whorl, which is an ideal environment for rust infection to take place. Or it may be a result of changes in the leaf tissue as it ages. New leaf tissue is more succulent and the cell walls are incompletely developed (Davis et al., 1995). The age of a particular leaf varied among plants of different environments at time of inoculation, and so did the effectiveness of the artificial inoculation. The mechanisms underlying the effect of leaf aging on rust are unknown.


View this table:
[in this window]
[in a new window]

  		Table 3. Means of percent leaf area damaged by rust for cycles of Minn11 sweet corn divergently selected for last leaf with epicuticular wax for three developmental stages, and seven leaves, averaged over three environments.

 
Cycles differed in percentage leaf area damaged by rust (Table 3). Cycle by environment interaction was significant but was the result of changes in magnitude not in rank. Percentage leaf area damaged by rust was greater in C3L and C2L than in C0, C1E, and C2E. There were no differences among C0, C1E, C2E, and C3E.

Inoculation at the v10 developmental stage resulted in the greatest separation among cycles compared with inoculation at v5 or v15 (Table 3). This further supports the concept that amount of leaf area damaged by rust was affected by developmental stage and the age of the leaf at the time of infection. In all developmental stages, differences among cycles were greatest in lower leaves and the differences declined acropetally (Fig. 1 ). Selection for late onset of the adult phase resulted in increased susceptibility to common rust. When plants were inoculated at the v5 stage, there were significant linear trends over cycles in the late direction for leaves 7, 8, 9, and 10 (Table 3). When inoculated at v10, there were significant linear trends on leaves 7, 8, and 9. While among cycles inoculated at v15, there were significant linear trends in leaves 9 and 10 (Table 3). C3L had significantly more leaf area damaged by rust than either C0 or C3E over nearly all leaves and timing of inoculation. The average increase in area damaged by rust per cycle in the late direction averaged over leaves with significant linear trends inoculated at v5 was slightly under 7%. At v10 the average increase was slightly under 8%, and at v15 the average increase was slightly under 7%. These increases in area damaged by rust were remarkable considering that the population was selected specifically for late onset of adult phase and not for increased susceptibility to common rust. There were no linear trends for response to common rust in the early direction (Table 3).


Figure 1
View larger version (20K):
[in this window]
[in a new window]

  		Figure 1. Percentage rust damage on individual leaves from each cycle of selection for early or late phase change in the Minn11 population of sweet corn when inoculated at the v10 stage of development and averaged over three environments.

 
Last leaf with juvenile wax was 12 in C3L and 10 in C0. Epicuticular wax in transition leaves is produced in the margins and toward the tip of leaf. The last leaf with epicuticular wax produces epicuticular wax only on the very tip (Bongard-Pierce et al., 1996). Consequently, leaves 8 and 9 in C3L are mostly juvenile while in C0 they are almost all adult. Thus, increased susceptibility in the late cycles on leaves 7, 8, and 9 was related to differences in leaf area covered by wax. Last leaf with epicuticular wax in C3E was leaf 8. The first leaf with adult wax in both C3E and C0 was leaf 7. Therefore, these cycles may have had similar amounts of adult and juvenile tissue in leaf 7. The main difference between C0 and C3E is that C3E had a narrower transition.

There was a significant linear response for the selected trait, last leaf with juvenile wax, in the early and late directions of selection. Response to selection in the adult vegetative trait, first leaf with adult wax, occurred after two cycles of selection in the early and late directions. In certain leaves and for certain times of inoculation, there were differences among cycles for area damaged by rust. Significant linear trends for area damaged by rust occurred only in the cycles selected for late transition. Increase in last leaf with juvenile wax, first leaf with adult wax, and area damaged by rust over cycles of selection in the late direction suggests an extension of the juvenile vegetative phase. The results of this study suggest that the timing of vegetative phase change may be associated with resistance to early infection by common rust in the population Minn11. In this population, juvenile tissue is clearly more susceptible than adult tissue. These results are also consistent with those of Abedon and Tracy (1996), who found that Cg1, a heterochronic mutation that has an elongated juvenile vegetative phase change and transition zone, was associated with increased susceptibility to infection by common rust relative to wild-type.


   ACKNOWLEDGMENTS
 
We thank the College of Agricultural and Life Sciences, University of Wisconsin-Madison for supporting this research and Dr. Jerald K. Pataky for supplying inoculum.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.

Received for publication August 28, 2007.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 





This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF) Free
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Basso, C. F.
Right arrow Articles by Tracy, W. F.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Basso, C. F.
Right arrow Articles by Tracy, W. F.
Agricola
Right arrow Articles by Basso, C. F.
Right arrow Articles by Tracy, W. F.
Related Collections
Right arrow Crop Growth and Development
Right arrow Crop Genetics

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
The SCI Journals Agronomy Journal Vadose Zone Journal
Journal of Natural Resources
and Life Sciences Education		 Soil Science Society of America Journal
Journal of Plant Registrations Journal of
Environmental Quality		 The Plant Genome