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Published online 23 September 2005
Published in Crop Sci 45:2240-2245 (2005)
© 2005 Crop Science Society of America
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CROP BREEDING, GENETICS & CYTOLOGY

Comparative Effects of the Sorghum bmr-6 and bmr-12 Genes

II. Grain Yield, Stover Yield, and Stover Quality in Grain Sorghum

A. L. Olivera, J. F. Pedersenb,*, R. J. Grantc, T. J. Klopfensteina and H. D. Josed

a Dep. of Animal Science, Univ. of Nebraska-Lincoln, Lincoln, NE 68583-0908
b USDA-ARS, NPA Wheat, Sorghum and Forage Research, Dep. of Agronomy, Univ. of Nebraska-Lincoln, Lincoln, NE 68583-0937
c W.H. Miner Agric. Res. Institute, Chazy, NY 12921
d Dep. of Agricultural Economics, Univ. of Nebraska-Lincoln, Lincoln, NE 68583-0922

* Corresponding author (jfp{at}unlserve.unl.edu)


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Nearly 3 million hectares of grain sorghum [Sorghum bicolor (L). Moench] are harvested in the USA each year. It may be possible to add value to crop and animal systems by enhancing the digestibility of the stover residue by the use of brown midrib (bmr) genes if grain yields can be maintained. The objectives of this study were to evaluate the effect of bmr-6 and bmr-12 genes on grain yield of sorghum and to evaluate the effect of the bmr genes on stover yield and quality in these genetic backgrounds: ‘Wheatland’, ‘Redlan’, RTx430, Tx623, Tx630, Tx631, and the hybrid AWheatland x RTx430. Plant height, maturity, grain yield and test weight, stover neutral detergent fiber (NDF), acid detergent fiber (ADF), acid detergent lignin (ADL), and in vitro NDF digestibility (IVNDFD) were measured in split-plot experiments replicated four times in each of four environments with lines being whole-plots and genotypes being subplots. Brown midrib genes reduced grain yield and residue yield in the lines; however, yield reduction was not observed in the bmr-12 AWheatland x RTx430 hybrid. The bmr-12 near-isolines generally had lowest stover lignin content and highest fiber digestibility, bmr-6 was intermediate, and wild-type counterparts had highest lignin content and lowest fiber digestibility. When all data are considered, the bmr-12 gene appears superior to the bmr-6 gene in terms of potentially adding value to the stover of grain sorghum for use in crop/animal systems. The variable expression of bmr-12 and bmr-6 in different lines indicates that selection of compatible genetic backgrounds will be critical in determining the realized impact on value.

Abbreviations: ADF, acid detergent fiber • ADL, acid detergent lignin • bmr, brown midrib • DM, dry matter • IVNDFD, in vitro neutral detergent fiber digestibility • NDF, neutral detergent fiber


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
MAIZE (Zea mays L.) crop residues often serve as an economical feed for ruminant animals (Klopfenstein et al., 1987). Nearly 3 million hectares of grain sorghum are harvested in the USA each year (USDA NASS, 2004), yet little research effort has been invested in the enhancement of grazing value of grain sorghum stover residue. There is less digestible organic matter found in sorghum stover than maize stover (Irlbeck et al., 1991). The DM digestibility of sorghum stover, as well as the crude protein content, is low when compared with maize stover (Osafo et al., 1997). Subsequently, when given the choice, producers choose to graze maize stalks. However, in some parts of the U.S. environmental conditions are not conducive to growing maize. Therefore, enhancing the quality of grain sorghum stover may offer an opportunity to add value to the overall system when post grain harvest stover residue is used as a forage base for livestock.

Chemical and genetic approaches have been employed to improve forage fiber digestibility by reducing the amount of lignin or the extent of lignin cross linked with cell wall carbohydrates. Brown midrib forage genotypes usually contain less lignin and may have altered lignin chemical composition (Bucholtz et al., 1980; Cherney et al., 1991; Vogel and Jung, 2001). Activities of two separate enzymes involved in lignin synthesis are reduced as the result of the bmr mutations bmr-6 (reduced cinnamyl alcohol dehydrogenase downregulation) (Bucholtz et al., 1980) and the allelic (Bittinger et al., 1981) bmr-12 and bmr-18 (reduced caffeic acid O-methyl transferase activity) (Bout and Vermerris, 2003). To date, genetic control of the lignification process through use of bmr genes has offered the most direct and productive approach to reducing lignin concentration and increasing digestibility of sorghums (Gerhardt et al., 1994).

The bmr phenotype is generally associated with reduced vigor and yield. Previous research in maize has demonstrated reductions of both the grain and stover yield (Lee and Brewbaker, 1984; Miller et al., 1983) of bmr maize compared with wild-type maize. Our research with near-isogenic forage sorghum demonstrated decreased average total DM yield in bmr forage lines (Oliver et al., 2005). However, in that study significant line x gene interactions were detected, with bmr-6 or bmr-12 near-isolines being equivalent in total biomass yield to their wild-type counterpart in three of the four grain sorghum genetic backgrounds studied.

In a previous forage sorghum study we reported increased fiber digestibility associated with mature bmr-6 and bmr-12 forage sorghum (Oliver et al., 2005). The effects of bmr genes on grain yield of grain sorghum, and the effect on quality of post grain harvest stover residue are unknown. It may be possible to add value to total crop/animal systems by enhancing the digestibility of the stover residue if grain yields can be maintained at acceptable levels. Therefore, the objectives of this study were to evaluate the impact of the bmr-6 and bmr-12 genes on the grain yield of grain sorghum and to evaluate impact of the bmr genes on the yield and quality of the post grain harvest stover residue.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Except where methods differed from Oliver et al. (2005), only a brief description is provided for the reader's convenience. For detailed descriptions of all materials and methods used in this study, the reader is referred to Oliver et al. (2005).

Near-isogenic versions of six common grain sorghum lines (Wheatland, Redlan, RTx430, Tx623, Tx630, Tx631) were created by crossing each to N121 (Gorz et al., 1990), a bmr-6 source, and F220 or F324 (donated to our project by the late Robert Kalton), bmr-12 sources, followed by three or four backcrosses. Near-isogenic versions of the grain sorghum hybrid AWheatland x RTx430 were also produced following male-sterilization of the bmr-6 and bmr-12 Wheatland using the A1 cytoplasmic male-sterility system. Field trials using the recurrent parents and their counterparts near-isogenic bmr-6 and bmr-12 lines, and the near-isogenic hybrids, were conducted in 2002 and 2003 at the University of Nebraska Field Laboratory, Ithaca, NE (Sharpsburg silty clay loam; fine, smectitic, mesic Typic Argiudoll), and Lincoln, NE [Kennebec silt loam (fine-silty, mixed, superactive mesic Cumulic Hapludoll)]. Nitrogen fertilizer was applied preplant at both locations at 157 kg ha–1. Individual plots consisted of two 7.6-m rows spaced 76 cm apart. Each was seeded with a precision vacuum planter calibrated to deliver 240 seeds per plot. Material was planted 20 May 2002 and 21 May 2003 in Lincoln and 22 May 2002 and 2003 in Ithaca. No supplemental irrigation was applied at Lincoln. Five centimeters of supplemental irrigation was applied at Ithaca via overhead sprinklers on 24 and 28 June and 5 and 7 August in 2002. In 2003 2.5 cm of supplemental irrigation was applied on 24 July and 14 and 28 August, and 5 cm of supplemental irrigation was applied on 4 and 7 August. Chemical application for weed and insect control was as described in Oliver et al. (2005)

Days to flowering was recorded at 50% anthesis. Height was measured to the top of the mature panicle before harvest. Panicles were hand-harvested at maturity then residue was harvested using a commercial silage cutter modified for small plot use (Pedersen and Moore, 1995). Grain and residue in the Ithaca plots were harvested 18 October 2002 and 3 to 4 October 2003. Grain and stover residue were harvested at Lincoln 6 September 2002, and 2 October 2003.

Sample Collection and Analysis
Grain samples were air dried to uniform 14% moisture, threshed, weighed, and test weight determined using a small plot combine with automated weight and test weight functions as a stationary thresher. Stover residue samples were collected and oven dried (60°C), DM content determined, ground through a Wiley mill (1-mm screen; Arthur H. Thomas Co., Philadelphia, PA), and analyzed sequentially for NDF, ADF, and ADL using an ANKOM 200 fiber analyzer (ANKOM Tech. Corp., Fairport, NY) (Vogel et al., 1999). In vitro NDF digestion (IVNDFD) was performed using ANKOM rumen fermenters (Model No: Daisy II; ANKOM Tech. Corp., Fairport, NY).

Statistical Analysis
Experimental design was a split-plot replicated four times in each of four environments with lines being whole-plots and genotypes (wild type, bmr-6, and bmr-12) being subplots. The data were analyzed using the PROC MIXED procedure of SAS (1999). The model statement included line, gene, and the line x gene effects. Environments and replication were considered random. The REPEATED function of PROC MIXED was used to account for lack of homogeniety of variance among the environments. F-protected least significant differences were used to determine differences among lines and genes (SAS, 1999). In the hybrid grain sorghum experiment, line was not included in the model.


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
There was a significant effect of the environment on the measured traits as expected, but because our objective was to determine the effects of the bmr genes across multiple environments and multiple genetic backgrounds, we accounted for environment and line in our model and report the pooled gene and gene x line means. Lodging was not observed in any of the bmr grain sorghum near-isolines or the bmr near-isogenic hybrids.

Grain Sorghum Lines
Brown midrib gene effects and gene x line effects were significant for maturity and height. Maturity of the bmr-12 near-isolines averaged 4 d later than the wild types and 3 d later than bmr-6 near-isolines (Table 1). In all genetic backgrounds, the bmr-12 near-isolines were later in maturity than the wild-type counterparts. The bmr-6 near-isolines were later maturing than Wheatland, Redlan, RTx430, and Tx630 wild-type counterparts, but earlier maturing than Tx623 and Tx631 wild-type counterparts. The bmr-6 near-isolines were consistently shorter than their bmr-12 or wild-type counterparts with a 9% average reduction in height. The bmr-12 near-isolines were equal in height to wild-type Wheatland, shorter than wild-type Tx623, Tx630, and Tx631, and taller than Redlan and RTx430 wild-type counterparts.


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  		Table 1. Average and individual effect of brown midrib (bmr) genes on maturity, height, and grain traits in six grain sorghum lines.

 
Line x gene interactions were not significant for grain yield. Wild-type lines averaged 6149 kg ha–1, or 20% higher grain yield than their bmr-6 near-isoline counterparts (5135 kg ha–1) and 24% more than their bmr-12 near-isogenic counterparts (4948 kg ha–1). Individual wild-type lines yielded more than either of their bmr near-isogenic counterparts in all genetic backgrounds. These reductions in grain yield are consistent in magnitude with those observed in maize hybrids. Previous research demonstrated a decrease in grain yield due to a bmr gene in maize (Miller et al., 1983). More specifically, in 15 pairs of isogenic hybrids, the grain yield of bm3 maize was 20% less than the wild type (Lee and Brewbaker, 1984). The bmr-6 near-isolines had significantly higher average grain yield than their bmr-12 counterparts.

Test weight of the grain was affected by the bmr genes with the wild type and their bmr-12 near-isoline counterparts being equivalent and averaging 731 kg m–3 and 735 kg m–3, respectively. The bmr-6 near-isolines were less dense, averaging 723 kg m–3. Line x gene interactions were significant. Test weights were equivalent for wild-type Wheatland, Redlan, RTx430, and Tx630 and their near-isogenic bmr-6 counterparts. In Wheatland, Redlan, RTx430, and Tx623 the bmr-12 near-isolines were denser than the wild-type counterparts. In Tx630 and Tx631, the wild type had higher test weight than the bmr-12 near-isoline counterparts. Although differences (P ≤ 0.05) were statistically significant for grain test weight, the differences were of little practical consequence with all but one line x gene combination (Tx631 bmr-6) meeting standards for U.S. number 2 sorghum.

Following grain harvest, the bmr-12 near-isolines had the highest stover residue DM yields (6503 kg ha–1), averaging 11% more stover residue DM than the wild type (5883 kg ha–1) (Table 2). The bmr-6 near-isolines averaged 10% less stover residue DM yield (5284 kg ha–1) than the wild type. Line x gene interactions were significant. In RTx430, stover residue DM yields ranked as above. In Wheatland, Tx623, and Tx631, bmr-12 near-isolines and their wild-type counterparts had equivalent stover residue DM yields and all had higher stover residue DM yields than their bmr-6 counterparts. In Tx630 and Redlan, the bmr-12 near-isoline had highest stover residue yield, and the bmr-6 near-isoline and wild type had equivalent stover residue yield.


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  		Table 2. Average and individual effect of brown midrib (bmr) genes residue traits in six grain sorghum lines.

 
The literature is mixed on the effect of the bmr trait on DM yield. Previous research in maize has indicated a similar relationship in stover yield in isogenic bm3 and the wild-type counterpart (Weller et al., 1985). In isogenic sudangrass [Sorghum x drummondii (Steud.) Millsp. & Chase], bmr-6 isolines counterparts had up to a 30% reduction in yield compared with the wild type (Casler et al., 2003), partially attributable to reductions in ground cover and tiller number. Dry matter yield in maize was also found to be lower in isogenic bm3 lines by Allen et al. (1997) and Gentinetta et al. (1990). Conversely, Singh et al. (2003) reports 11 various bmr genotypes had greater yield than nine wild-type nonisogenic sorghums. The bmr-12 near-isolines in our study consistently yielded equivalent or more stover residue DM than wild type or bmr-6 counterparts.

Line x gene interactions were significant for NDF concentration of grain sorghum stover residue. Wild-type Wheatland and Tx631 had significantly higher NDF concentration than their bmr-6 or bmr-12 counterparts, which were equivalent in NDF concentration. Wild-type Tx623 had significantly more NDF concentration than its bmr-6 near-isogenic counterparts and was equivalent in NDF concentration to its bmr-12 near-isogenic counterpart. In Tx630, the bmr-6 near-isoline had the highest NDF concentration. In Redlan and RTx430 no differences due to bmr genes were detected. Research by Thorstensson et al. (1992) also found wild-type sorghum to have higher NDF concentration when compared to its bmr-6 counterpart. The same study found no differences in the NDF concentration of bmr-18 and its normal isogenic counterpart. Other studies have not found a difference in the NDF concentration of bmr forage sorghums and conventional forage sorghums (Aydin et al., 1999; Ruiz et al., 1995). As in our previous forage sorghum study (Oliver et al., 2005), NDF concentration appears to be quite variable in various lines and line x bmr gene combinations.

Of perhaps greater importance in predicting animal response and formulating rations, stover residue ADF content was equivalent or greater for the wild-type near-isolines than the bmr counterparts in the grain sorghum lines in the current study. Averaged across lines, the wild type had highest ADF content (379 g kg–1) with bmr-6 near-isolines intermediate (365 g kg–1), and bmr-12 near-isolines having lowest ADF content (354 g kg–1). In Wheatland, Redlan, and Tx623, bmr-12 near-isolines had lower ADF content than wild type and equivalent ADF content to bmr-6 counterparts. Tx630 bmr-6 had greater ADF content than its wild type and bmr-12 counterpart. Tx631 wild type had the highest ADF content, its bmr-6 counterpart intermediate, and its bmr-12 counterpart lowest ADF content. No differences in ADF content were attributable to bmr genes in RTx430. Previous research using nonisogenic forage sorghum has shown bmr genotypes to have reduced ADF concentration compared to conventional wild-type sorghum (Oliver et al., 2004) while other research has indicated similar ADF concentration among bmr and wild-type lines (Aydin et al., 1999). Initial research on the fiber content of sorghum has found it to vary greatly (Porter et al., 1978). We can surmise that the fiber content of sorghum stover residue varies greatly depending on the line as well as the genotype due to the significance of both the gene and lines.

The bmr genes are best known for their ability to reduce the amount of lignin in the stover portion of sorghum and maize. Line x gene interactions were not significant for ADL concentration of stover residue in the current study. The bmr-12 near-isolines had the lowest ADL concentration (67 g kg–1) averaging 34% less ADL concentration than wild-type counterparts (91 g kg–1) and 14% less than their bmr-6 counterparts (77 g kg–1). These results concur with our previous research on forage hybrids (Oliver et al., 2004) and other previous research in sorghum and maize which showed a reduction in ADL concentration of bmr genotypes (Gerhardt et al., 1994; Lam et al., 1996; Miller et al., 1983; Thorstensson et al., 1992). Our results are unique, however, in comparing ADL concentration of mature-plant stover residue samples (grain fraction removed) of bmr-6 and bmr-12 near-isogenic pairs. The ADL concentration of the bmr-6 isolines averaged 15% higher than their bmr-12 counterparts, and ADL concentration of bmr-6 lines was intermediate to the ADL concentration of their wild type and bmr-12 near-isogenic counterparts.

The IVNDFD of the grain sorghum residue followed the inverse pattern as the ADL concentration. The IVNDFD of stover residue averaged across lines was 10% greater in bmr-12 near-isolines (556 g kg–1) than in the wild-type counterparts (505 g kg–1), and 6% greater than the bmr-6 counterparts (526 g kg–1). IVNDFD line x gene effects were significant. In all the genetic backgrounds the bmr-12 near-isolines had IVNDFD equal to or greater than their bmr-6 or wild-type counterparts. In Wheatland and Tx623 the bmr-12 near-isolines had the highest IVNDFD, the bmr-6 intermediate, and wild type the lowest IVNDFD. In Redlan, no differences in IVNDFD were detected between bmr-6 and bmr-12 near-isolines, and the wild type was significantly less digestible. In Tx631, Tx630, and RTx430 the bmr-6 near-isolines and wild-type counterparts did not differ in IVNDFD and both had lower IVNDFD than their bmr-12 counterparts. These results are similar to previous studies in which bmr genotypes were shown to have increased IVDMD in sorghum silage (Akin et al., 1986; Cherney et al., 1986; Fritz et al., 1988; Porter et al., 1978). However, those prior studies did not directly compare effects bmr genes in multiple genetic backgrounds.

Grain Sorghum Hybrid
Gene effects were significant for all traits measured in the AWheatland x RTx430 grain sorghum bmr near-isogenic hybrids. The bmr-12 near-isogenic hybrid was 14 cm taller and 4 d later in maturity than the wild-type hybrid (Table 3). The bmr-6 near-isogenic hybrid was 8 cm shorter than the wild type and 1 d later in maturity. Grain test weight was highest in the bmr-12 near-isogenic hybrid, with the bmr-6 near-isogenic hybrid, and the wild type being equivalent.


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  		Table 3. Average and individual effect of brown midrib (bmr) genes on grain and residue traits in the grain sorghum hybrid AWheatland x RTx430.

 
There was no statistically significant difference (P = 0.05) in the grain yield of the bmr-12 near-isogenic hybrid (7549 kg ha–1) and its wild-type counterpart (7629 kg ha–1). Grain yield was reduced 11% in the bmr-6 near-isogenic hybrid (6826 kg ha–1). Lee and Brewbaker (1984) stated the decrease in maize grain yield in bmr hybrids could be overcome by selection due to the significant genotype x hybrid interaction. Although our results are based on only one hybrid, these results suggest that in sorghum the effect of selective breeding and heterosis may overcome the grain yield-drag associated with bmr. It should be noted that the bmr-12 near-isogenic hybrid was 4 d later in maturity, and 14 cm taller than the wild-type hybrid. Increased days to maturity and height are both positively associated with grain yield, but it is doubtful that the minor changes noted in height and maturity overcame the yield reduction associated with bmr-12 in inbred sorghum lines. The equivalent grain yield of the AWheatland x RTx430 hybrid and its bmr-12 near-isogenic counterpart suggest that bmr grain sorghum hybrids can be developed with equivalent grain yield to wild-type grain sorghum hybrids.

The bmr-12 near-isogenic hybrid yielded 10% more stover residue DM (7039 kg ha–1) than the wild type (6405 kg ha–1). The bmr-6 near-isogenic hybrid yielded 13% less stover residue DM (5542 kg ha–1) than the wild type. The bmr-12 and wild type near-isogenic hybrids had equivalent stover residue NDF concentration (628 g kg–1, and 620 g kg–1, respectively) and both had higher NDF concentration than the bmr-6 near-isogenic hybrid (603 g kg–1). The bmr-6 near-isogenic hybrid had lowest stover residue ADF concentration (351 g kg–1), and the bmr-12 and wild-type near-isogenic hybrids were equivalent in stover residue ADF content (379 g kg–1 and 382 g kg–1, respectively). The bmr-12 hybrid had 33% less stover residue ADL (65 g kg–1) than the wild type (96 g kg–1) and 11% less ADL concentration than the bmr-6 near-isogenic hybrid (72 g kg–1). The IVNDFD of the bmr-6 and bmr-12 near-isogenic hybrids were equivalent (544 g kg–1 and 537 g kg–1, respectively), and 7 to 9% greater than the wild-type hybrid stover residue (501 g kg–1).

In conclusion, bmr genes have negative agronomic impact on grain yield and residue yield in grain sorghum lines. However, it appears that these negative impacts can be overcome by heterosis in sorghum as evidenced by the grain and residue yields of the AWheatland x RTx430 bmr-12 hybrid used in this study. Hanna et al. (1981) drew the conclusion that bmr-12 was the superior bmr gene in sorghum. Results from this study generally agree with that conclusion, but also demonstrate the variable expression of bmr-12 and bmr-6 in different genetic backgrounds. When all data are considered in aggregate, the bmr-12 gene appears superior to the bmr-6 gene in terms of potentially adding value to grain sorghum for use in grain production/animal forage systems.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Joint contribution of the USDA-ARS and the Univ. of Nebraska Agric. Exp. Stn. as Paper no. 171865, Journal Series, Nebraska Agric. Exp. Stn.

Received for publication November 15, 2004.


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




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