The plasticity of the oat panicle and associated changes in leaf area and grain weight

Field Crops Research 242 (2019) 107592

Contents lists available at ScienceDirect

Field Crops Research journal homepage: www.elsevier.com/locate/fcr

The plasticity of the oat panicle and associated changes in leaf area and grain weight

T

John Finnan , Brendan Burke, John Spink ⁎

Crops Research Department, Crops, Environment and Land Use Programme, Teagasc, Oak Park, Carlow, Ireland

ARTICLE INFO

ABSTRACT

Keywords: Oats Panicle Plasticity Whorl Grain weight Leaf area

The objective of the current investigation was to study the plasticity of the oat panicle together with associated changes in leaf area and grain weight as affected by seed rate and tiller order. Plants (cv. Husky) were sampled from autumn sown seed rate experiments (100, 200, 300, 400, 500 seeds/m2) in 2016 and 2017 after anthesis and separated into their component tillers. The number of primary, secondary and tertiary grains on each whorl of the panicle of each tiller were counted, green leaf area per tiller was measured and, in 2017, the number of green leaves per shoot in addition to leaf length and leaf width were measured. At grain maturity, plants were sampled from three treatments (100, 300, 500 seeds/m2) and separated into their component tillers. The number of primary, secondary and tertiary grains on each whorl were counted and weighed. Primary and secondary grain numbers on all mainstem whorls except the uppermost whorl increased significantly as seed rate decreased, the largest changes being on the bottom whorls. There were also significant increases in green leaf area per stem as seed rate was decreased due to increases both in the number and size of leaves. Grain numbers per whorl decreased significantly with increasing tiller order but green leaf number per stem and leaf area per grain increased with increasing tiller order. The number of secondary grains per panicle was tightly correlated with the number of primary grains per panicle irrespective of seed rate or tiller order. Seed rate had no significant effect on the weight of primary or secondary grains but primary and secondary grain weights were significantly greater on the first tiller compared to the mainstem and second tiller. The oat panicle is a highly plastic organ, the plasticity of the oat panicle contributes to yield stability. Grain weight stability is preserved across a wide range of panicle sizes by changes in leaf area per stem and by the highly stable nature of the relationships between primary and secondary grain numbers and between primary and secondary grain weight.

1. Introduction Interest in the use of oats in the human diet is growing because of a new appreciation of the nutritional and health benefits of oat consumption. The Food and Drug Administration in the United States has accepted a health claim stating that a daily intake of 3 g of soluble oat β-glucan can lower the risk of coronary heart disease (US FDA, 1997). Recently, Ryan et al. (2017) suggested that oat β-glucan may be the preferred dietary intervention for safe, long-term maintenance of cardiovascular and metabolic health. Additionally, the protein composition of oats allows most coeliac disease patients to safely consume oats which are not contaminated by other cereals (Clemens and van Klinken, 2014; Thies et al., 2014). However, agronomic research on oats has lagged behind research on other cereal crops. Consequently, knowledge on how to optimise oat grain yield and its components lags behind other crops yet the individual components of yield impose constraints on

⁎

plant form and are frequently barriers to improving yield (Grafius, 1978). The grain yield of a cereal crop can be split into three major components; ear population density, ear size and individual grain weight (Hay and Walker, 1989). A recent focus on phenotypic plasticity has brought fresh perspective to the relationships between the different yield components (Sadras, 2007; Peltonen-Sainio et al., 2011; Sadras and Slafer, 2012; Slafer et al., 2014). Plasticity refers to the amount by which a morphological or physiological attribute of an individual genotype can be modified by its environment (Bradshaw, 1965). Plasticity is a major mechanism which allows crops to achieve yield stability in variable environments (Kumar et al., 2017). Hierarchies of plasticities occur within species with plastic traits typically being associated with more stable traits, Sadras and Slafer (2012) suggested the following hierarchy of plasticity in cereals – tiller number > inflorescence number ∼ grains per inflorescence > seed size. Slafer

Corresponding author. E-mail address: [email protected] (J. Finnan).

https://doi.org/10.1016/j.fcr.2019.107592 Received 30 April 2019; Received in revised form 11 August 2019; Accepted 12 August 2019 Available online 22 August 2019 0378-4290/ © 2019 Elsevier B.V. All rights reserved.

Field Crops Research 242 (2019) 107592

J. Finnan, et al.

et al. (2014) subsequently reported that the plasticity of inflorescence number was greater than that of the number of grains per inflorescence in wheat. However, this hierarchy of plasticities is inverted in oats where the plasticity of the number of grains per inflorescence exceeds that of inflorescence number (Mahadevan et al., 2016: Finnan et al., 2019). Evidence of the plasticity of the oat panicle also comes from findings that panicle weight is closely related to grain yield (PeltonenSainio, 1990, 1994) and from agronomic experiments where large changes in the number of grains per panicle have been reported (Finnan et al., 2018, 2019; Jones and Hayes, 1967; Peltonen-Sainio, 1997; Peltonen‐Sainio and Järvinen, 1994). Yield tends to be more closely related to the number of grains per land area (ear population density by the number of grains per ear) rather than to individual grain weight (Gallagher et al., 1975; Gales, 1983; Peltonen-Sainio et al., 2007). It has been proposed that the relatively narrow range of seed size within any species results from both evolutionary and agronomic selection (Sadras, 2007). Additionally, lower plasticity can be expected from yield components whose magnitude is determined later in the growing season (Sadras and Slafer, 2012; Kumar et al., 2016). The ability of cereal plants to utilise preanthesis assimilate for grain filling also helps to maintain stable grain weight particularly under adverse environmental conditions (Gallagher et al., 1975). Additionally, an increase in the number of grains per shoot can be accompanied by increased green leaf area per shoot producing more assimilates per shoot to support larger grain numbers (Kirby and Faris, 1972; Whaley et al., 2000). Although grain weight is the most stable of yield components (Gales, 1983; Peltonen-Sainio et al., 2007; Sadras and Slafer, 2012; Slafer et al., 2014), changes in grain weight do occur between seasons, treatments and plant parts (Finnan et al., 2018; Darwinkel, 1978; McLaren, 1981). Furthermore, the grain weight of any individual treatment, expressed as thousand grain weight, consists of a range of individual grain weights as the weight of a cereal grain can change with tiller order (Darwinkel, 1980), location of the grain within the inflorescence (Doehlert et al., 2002; White and Finnan, 2017) and floret type (Rajala and Peltonen-Sainio, 2004). A wide range of phenotypic plasticity is generally evident when cereal plants are grown at different plant densities. Cereal species, including oats, are able to ensure yield stability across a wide range of plant densities without compromising grain weight through variations in plant form (Conry and Hegarty, 1992; Spink et al., 2000; Finnan et al., 2018). In a previous seed rate study on autumn sown oats, differences in grain numbers between seed rate treatments were minimised, largely, through changes in the plasticity of the oat panicle while there were no significant differences in thousand grain and only small differences in radiation interception between treatments (Finnan et al., 2018). The studies described in this paper were conducted on the seed rate trials detailed in Finnan et al. (2018). Whereas, the effect of seed rate at the crop level were described in Finnan et al. (2018), the focus of this study was to quantify the effects of seed rate at the level of individual tillers and at the level of individual panicle whorls. The study of phenotypic plasticity in oats is important as plasticity determines the ability of a genotype or species to adapt to environmental conditions such as resource limitation and stress. Hence, our study of the effect of seed rates on the plasticity of the oat plant should contribute to a better understanding of plasticity in oats. Our overall objective was to quantify changes in leaf area, panicle plasticity and grain weight across different seed rates on individual tillers and on individual panicle whorls.

(Barra, Husky and Vodka) and there were four replicates of each treatment. Full details are provided in Finnan et al. (2018). 2.1. Changes in panicle plasticity and leaf area per stem After anthesis (GS 75; Zadoks et al., 1974) in the 2016 and 2017 growing seasons, ten plants were sampled at random from each of the plots of Husky from the seed rate experiment conducted on the light soil type. Individual stems of each plant were separated by increasing tiller order (mainstem, tiller 1, tiller 2 etc) as defined by Power and Alessi, 1978. Green leaves were separated, green leaf area was measured using a WINDIAS leaf image analysis system (Delta T Devices Ltd, 130 Low Road, Burwell, Cambridge, United Kingdom) and green leaf area per stem estimated. Additionally, in 2017, the numbers of green leaves per stem (leaves with > 40% green leaf area) were counted and the length and width of each green leaf was measured. The panicles corresponding to each stem were separated into whorl components; whorl 1 being at the bottom of the panicle. The number of single grained spikelets (primary grain only), double grained spikelets (primary and secondary grains) and the number of triple grained spikelets (primary, secondary and tertiary grains) were counted on each whorl and the number of primary, secondary and tertiary grains per whorl and per panicle calculated. The ratio of primary grain numbers to secondary grain numbers was also calculated for each whorl and for each panicle. Green leaf area per grain, per stem and per plant were also calculated from these measurements and total grain number were calculated for mainstem, tiller and whole plant for each seed rate. 2.2. Changes in grain weight In the 2016 and 2017 growing seasons, five plants were randomly sampled at physiological maturity (GS 91; Zadoks et al., 1974) from plots of the variety Husky at three different seed rates (100 seeds/m2, 300 seeds/m2, 500 seeds/m2) from the seed rate experiment conducted on the heavy soil type. Individual stems of each plant were processed to separate tillers by increasing tiller order (mainstem, tiller 1, tiller 2 etc). The panicle from each stem was separated into its component whorls and the primary, secondary and tertiary grains in the spikelets on each whorl were removed and the respective grain numbers counted for each whorl. The grains obtained were then dried to constant weight and weighed. Average individual grain weights for primary, secondary and tertiary grains on each whorl were calculated. The ratio of primary to secondary grain weight was also calculated for each whorl and panicle. 2.3. Data analysis Statistical analysis was used to compare mainstem and plant characteristics across seed rates and to compare the characteristics of different tillers. The tiller analysis was conducted on the component tillers of the lowest seed rate treatment (100 seeds/m2), three of the component tillers were included in this analysis (mainstem, tiller 1, tiller 2) as higher order tillers were not always present. This analysis included all four replicates, tiller was measured within plot so it was analysed as repeated effect within independent plots. The correlation between tillers measurements within plot was modelled using a compound symmetry covariance model. The Glimmix procedure in SAS 9.4 (SAS, 2014) was used for all of these analyses (mainstem, whole plant and tiller analysis) in which year, treatment and replicate were fixed factors. Pairwise differences in treatments were evaluated using Tukey’s honest significance difference test. Non-normal datasets were log transformed for the analysis before being back transformed at the end of the analysis. Linear regression analysis was used to quantify the relationship between primary and secondary grains. The GLM procedure in SAS 9.4 was used for this analysis.

2. Materials and methods Autumn sown seed rate experiment with five seed rates (100, 200, 300, 400, 500 seeds/m2) were conducted on two soil types (light and heavy soils) at Oak Park Research Centre, Carlow, Republic of Ireland (52.86 ° N, 6.90 °W) over three growing seasons(2015–2017). Seed rate was the main factor in the experiment, the second factor was variety 2

Field Crops Research 242 (2019) 107592

< 0.0001 0.0002 0.0001

3. Results 3.1. Changes in panicle plasticity and leaf area per stem

< 0.0001 0.4778 0.4102

< 0.0001 0.9737 0.2400

0.0003 0.6732 0.67

0.0134 0.9915 0.6687

0.1356 0.2664 0.2126

3.1.1. The effect of seed rate on mainstem parameters The effect of seed rate on the number of primary grains on each mainstem whorl is shown in Table 1. With the exception of the uppermost whorl (whorl 8), the number of primary grains per mainstem whorl significantly decreased with increasing seed rate from 100 seeds/ m2 to 500 seeds/m2. The effect of seed rate was greatest in the lower whorls of the panicle but decreased towards the top of the panicle. Increasing the seed rate from 100 seeds/m2 to 500 seeds/m2 had the effect of decreasing primary grain numbers in the bottom whorl (whorl 1) by over 75% whereas corresponding grain numbers in whorls 6 and 7 were decreased by approximately 25%. Similarly, there was a significant effect of seed rate on total primary grain numbers per panicle which decreased by approximately 60% as seed rate was increased from 100 seeds/m2 to 500 seeds/m2. Year had a significant effect on the number of primary grains in the bottom whorls of the panicle (whorls 1 and –2) but not on the number of primary grains on the middle and top whorls of the panicle or on the total number of primary grains per mainstem panicle. The number of primary grains in the bottom whorl of the panicle (whorl 1) was significantly greater in 2017 compared to 2016 whereas the number of primary grains in the second whorl (whorl 2) of the panicle was significantly greater in 2016 compared to 2017. Different rates of decline in grain numbers with seed rate between years resulted in significant interactions in whorls 1 and 2 and in the total number of primary grains per panicle (Table 1). The effect of seed rate, year and interactions on the number of secondary grains on each mainstem whorl were similar to the effects on primary grain numbers (Table 1). Changing the seed rate from 100 seeds/m2 to 500 seeds/m2 decreased secondary grain numbers in the bottom whorl (whorl 1) by over 75% whereas corresponding grain numbers in whorls 6 and 7 were decreased by approximately 25%. Total secondary grain numbers per panicle decreased significantly by approximately 60% with an increase in seed rate from 100 seeds/m2 to 500 seeds/m2. The number of secondary grains in whorl 1 and the total number of secondary grains per panicle in 2017 was significantly greater than in 2016. There were significant interactions between seed rate and year for the first two whorls and the total secondary grains per panicle due to different rates of decline in grain numbers per whorl between years. There was no significant effect of seed rate on the number of tertiary grains per mainstem panicle (data not shown). The number of tertiary grains per panicle were significantly greater in 2016 (average of 1.1 tertiary grains per panicle) compared to 2017 (average of 0.5 grains per panicle). The number of green leaves per mainstem as well as green leaf area per mainstem declined significantly as seed rate increased from 100 seeds/m2 to 500 seeds/m2 (Table 2). Seed rate also had a significant effect on leaf length and leaf width. Leaf length increased by 6.4 cm while leaf width increased by 0.6 cm when seed rate was reduced from 500 seeds/m2 to 100 seeds/m2. Seed rate had no significant effect on green leaf area per grain. However, the interaction between year and seed rate was significant; as leaf area per grain increased with seed rate up to 300 seeds/m2 in 2016 whereas, in 2017, the parameter was stable from 100 seeds/m2 to 300 seeds/m2 before declining at higher seed rates (Fig. S1).

< 0.0001 0.1107 0.1343

< 0.0001 0.2106 0.3110

< 0.0001 0.957 0.2424

0.0003 0.6725 0.7106

0.0134 0.9915 0.6687

0.1669 0.3145 0.2425

< 0.0001 0.2445 0.0020

< 0.0001 < 0.0001 0.0072

< 0.0001 0.1156 0.0036 < 0.0001 0.0245 0.0029 < 0.0001 0.0004 0.0030 Seed rate (SR) Year SR*Year

< 0.0001 0.6655 0.2288

58.6B 67.7A 0.9 1.0 1.6 1.6 2.8 2.8 4.9 4.9 9.2 9.0 15.9 14.8

9.6 9.1

5.0 5.0

2.8 2.8

1.6 1.6

0.9 1.0

66.8 70.1

7.1B 12.3A

13.8 14.8 17.2A 15.3B 9.7B 13.0A

14.3 14.5

95.3A 76.5B 58.6C 46.0D 39.2D 1.0 1.0 0.9 1.0 0.9 1.9A 1.8AB 1.6AB 1.4AB 1.4B 3.4A 3.2AB 2.6BC 2.6BC 2.2C 6.3A 5.4AB 4.8BC 4.4BC 3.8C 12.8A 10.8B 9.0C 7.6CD 6.5D 19.9A 13.1B 9.2C 6.1D 4.6D 104.6A 82.5B 62.6C 50.2DC 42.3D 1.0 1.0 0.9 1.0 0.9 1.9A 1.8AB 1.6AB 1.4AB 1.4B 3.4A 3.2AB 2.6BC 2.6BC 2.2C 6.4 A 5.5AB 4.8BC 4.4C 3.8C 13.4A 11.1B 9.2C 7.8CD 6.7D 22.3A 19.6A 15.0B 11.9C 10.7C

Total grains Whorl 8 Whorl 7 Whorl 6 Whorl 5 Whorl 4 Whorl 3

24.3A 18.7B 14.4C 10.2D 8.7D 28.0A 21.3B 15.9C 11.8D 9.8D 23.8A 15.6B 10.7C 7.5D 5.7D

Seed Rate 100 200 300 400 500 Year 2016 2017

20.8A 18.6A 14.2B 11.2C 10.1C

Total grains Whorl 8 Whorl 7 Whorl 6 Whorl 5 Whorl 4 Whorl 3 Whorl 1 Whorl 2 Whorl 1

Whorl 2

Secondary grain numbers Primary grain numbers

Table 1 The effect of seed rate (seeds/m2) on the number of primary and secondary grains on each mainstem whorl. Letters represent significant pairwise differences between levels within a factor, figures followed by the same letter are not significantly different. P values are indicated within the table.

J. Finnan, et al.

3.1.2. The effect of tiller order on stem parameters The number of primary grains per whorl (except the uppermost whorl 8) and per panicle significantly declined with increasing tiller order (Table 3). The number of primary grains in whorl 1 in 2017 was significantly higher than 2016 which in turn resulted in significant interaction of tiller order and year, while the years and interaction had 3

4

0.8 1.0 0.1241 0.0922 0.9204 1.4 1.7 0.0034 0.1869 0.3549 2.5 3.0 0.0014 0.1152 0.2856 4.4 5.3 0.0001 0.0317 0.7038 8.7 9.6 < 0.0001 0.3106 0.9861 12.9 14.9 < 0.0001 0.2011 0.9496 12.5B 16.9A < 0.0001 0.0217 0.1811 7.5B 15.2A < 0.0001 0.0087 0.0013

95.3A 49.6B 34.1C 1.0 0.9 0.7 1.9A 1.5B 1.3B 3.4A 2.5B 2.3B 6.3A 4.4B 3.8B 12.9A 8.1B 6.6B 20.9A 12.5B 8.3C 25.0A 12.3B 6.8C 22.8A 7.9B 3.5B

Total grains Whorl 8

15.4 18.7 < 0.0001 0.1328 0.7097 9.8B 16.9A < 0.0001 0.0237 0.0042

14.3 16.0 < 0.0001 0.3425 0.8608

9.2 9.9 < 0.0001 0.5253 0.9931

4.5B 5.4A 0.0002 0.0546 0.6637

2.5B 3.0A 0.0014 0.1437 0.2670

1.4B 1.7A 0.0051 0.2173 0.4478

0.8 1.0 0.1298 0.1027 0.9512

58.9 72.9 < 0.0001 0.0502 0.1466

Mainstem Tiller 1 Tiller 2 Year 2016 2017 Tiller Year Tiller*Year 104.6A 55.2B 37.9C 1.0 0.9 0.7 1.9A 1.5B 1.3B 3.4A 2.6B 2.4B 6.4A 4.5B 3.9B 13.5A 8.4B 6.8B 22.5A 13.8B 9.3C 28.5A 13.9B 8.7B

3.1.4. The effect of seed rate on plant parameters Seed rate had a significant effect (P < 0.0001) on the number of grains per plant which decreased from 332 grains/plant in the lowest seed rate treatment to 86 grains/plant in the highest seed rate treatment. The green leaf area per plant (P < 0.0001) significantly decreased from 277 cm2/plant to 65 cm2/plant in the lowest to highest seed rate treatment. Year and its interaction with seed rate did not have a significant effect on the above traits. In contrast, there was no significant effect of seed rate and year on green leaf area per grain but there was a significant interaction as this parameter decreased with seed rate in 2016 but increased with seed rate in 2017. Data for these parameters is shown in Fig. 5 (see Section 3.3 below) which shows the

26.3A 9.5B 4.2B

3.1.3. The relationship between primary and secondary grain numbers Seed rate had no significant effect on the ratio of primary grains to secondary grains in mainstem panicles (data not shown) or at any individual whorl with the exception of whorl 5 where seed rate had a significant effect (P < 0.05) although the difference between the highest and lowest ratio was very small (0.01). Similarly, tiller order had no significant effect on the ratio between primary and secondary grain numbers. The relationship between primary and secondary grain numbers per panicle for all tillers orders and seed rates is shown in Fig. 1. There were highly significant relationships between these two parameters in both years although there were small differences between years as there were higher number of secondary grains per panicle for the same number of primary grains per panicle in 2017 compared to 2016.

Mainstem Tiller 1 Tiller 2 Year 2016 2017 Tiller Year Tiller*Year

no difference in other whorls. The effect of tiller order on secondary grain numbers per whorl and per panicle was similar to the effect of tiller order on primary grain numbers (Table 3). The effect of year was significant at whorls 1, 2, 5 and on the total secondary grain numbers per panicle as there were significantly more grains in 2017 compared to 2016. There was no significant effect of tiller order on the number of tertiary grains per panicle (data not shown). The number of tertiary grains were significantly greater in 2016 comared to 2017. There was a significant decline in green leaf area per stem corresponding to reduction in leaf length and width with increasing tiller order (Table 4) and the interaction effect was significant (Fig. S2). However, leaf number and green leaf area per grain significantly increased with increasing tiller order.

Whorl 7

< 0.0001

Whorl 6

0.0006

Whorl 5

0.0169

Whorl 4

0.3717 0.0902 0.0377

Whorl 3

< 0.0001 0.4481 0.3943

Whorl 2

0.76 0.75

Whorl 1

96.1 91.6

Total grains

2.4A 2.3AB 2.1B 1.9C 1.8C

Whorl 8

34.7A 33.3A 30.9AB 27.9B 27.3B

Whorl 7

3.7A 3.5AB 3.3AB 3.1B 3.0B

Whorl 6

0.67 0.71 0.84 0.76 0.77

Whorl 5

125.8A 109.8A 101.0A 73.1B 59.7B

Whorl 4

Average leaf width (cm)

Whorl 3

Average leaf length (cm)

Whorl 2

Number of leaves per mainstem with green leaf material

Whorl 1

Seed Rate Year Seed rate * year

Green leaf area per grain (cm2)

Secondary grain numbers

Seed Rate 100 200 300 400 500 Year 2016 2017

Green leaf area per mainstem (cm2)

Primary grain numbers

Table 3 Number of primary grains and secondary grains on each whorl on the panicles of the mainstem, first tiller and second tiller of the 100 seeds/m2 seed rate treatment. Letters represent significant pairwise differences between levels within a factor, figures followed by the same letter are not significantly different. P values are indicated within the table.

Table 2 The effect of seed rate (seeds/m2) on mainstem leaf parameters. Letters represent significant pairwise differences between the levels within a factor, figures followed by the same letter are not significantly different. P values are indicated within the table.

51.2B 68.1A < 0.0001 0.0097 0.0284

Field Crops Research 242 (2019) 107592

J. Finnan, et al.

Field Crops Research 242 (2019) 107592

J. Finnan, et al.

mainstem tertiary grain weight was 12 mg (data not shown).

Table 4 The effect of tiller order on leaf parameters of the 100 seeds/m2 seed rate treatment. Letters represent significant pairwise differences between the levels within a factors, figures followed by the same letter are not significantly different. P values are indicated within the table. Green leaf area per stem (cm2)

Green leaf area per grain (cm2)

Leaf number per stem

Average leaf length (cm)

Average leaf width (cm)

Mainstem Tiller 1 Tiller 2 Year 2016 2017

125.8A 117.4A 97.5B

0.67B 1.18A 1.49A

3.7B 4.2AB 4.5A

34.7A 31.0A 26.0B

2.4A 2.0AB 1.7B

109.9 117.2

1.1 1.1

Tiller Year Tiller*Year

0.0041 0.6270 0.0086

0.0007 0.8742 0.1892

0.0144

0.0008

0.0057

3.2.2. The effect of tiller order on individual grain weight at 100 seeds/m2 Primary grain weight was higher on tiller 1 compared to the mainstem and tiller 2 (Fig. 3a). This difference was evident at all whorl positions although the difference was only significant at whorl 6 and on average primary grain weight. Year had a significant effect on average primary grain weight at each whorl position with the exception of the lowest whorl (whorl 1) as primary grain weight in 2016 was greater than primary grain weight in 2017. There were no significant interactions between year and tiller order. Secondary grain weight was higher on tiller 1 compared to the mainstem and tiller 2 (Fig. 3b). However, the difference was only significant on average secondary grain weight and not at any whorl position. Year had a significant effect on average secondary grain weight at all whorl positions with the exception of the lowest whorl and the uppermost whorl as secondary grain weight in 2016 was greater than secondary grain weight in 2017. There were no significant interactions between tiller order and year. Tiller order had no significant effect on tertiary grain weight, the average tertiary grain weight across all tillers was 12 mg (data not shown).

contribution of the plasticity of certain traits to the stability of other traits. 3.2. Changes in individual grain weight

3.2.3. The relationship between primary grain weight and secondary grain weight Seed rate had no significant effect on the ratio between primary and secondary grain weight across the whole panicle or at any whorl (average primary grain weight vs average secondary grain weight; data not shown). Year had no significant effect on the ratio between primary and secondary grain weight with the exception of whorl 1 and whorl 5. On whorl 1, the 2016 ratio was significantly greater than the 2017 ratio whereas the 2017 ratio was significantly greater than the 2016 ratio on whorl 5. There were significant interactions between seed rate and year at whorls 3, 4 and 5 but not at the other whorls or on whole panicle ratio. Interactions were due to the fact that the primary to secondary grain weight ratio of the 300 seeds/m2 treatment was higher than the other seed rate treatments in 2016 but lower in 2017. Tiller order had no significant effect on the ratio between primary and secondary grain weight across the whole panicle or at any whorl (average primary grain weight vs average secondary grain weight; data not shown). Year had a significant effect on the primary to secondary

3.2.1. The effect of seed rate on individual grain weight within mainstem panicles Seed rate had no significant effect on primary and secondary grain weight at any mainstem whorl position or on average mainstem primary or secondary grain weight (Fig. 2a & b). There was a significant effect of year on average grain weight at each whorl with the exception of the lowest whorl (whorl 1) for primary grain weight and for the two lowest whorls (whorls 1 and 2) and the uppermost whorl (whorl 8) for secondary grain weight. There was a significant interaction between year and seed rate on average primary grain weight and on primary grain weight at each whorl position with the exception of the lowest whorl while the interaction on secondary grain weight was significant at whorls 3, 4, 5, 6 and 7. The interaction was caused by the fact that primary and secondary grain weight from the 300 seeds/m2 treatment tended to be higher than the other seed rate treatments in 2017 but lower in 2016. Seed rate had no significant effect on tertiary grain weight, average

Fig. 1. The relationship between the number of primary grains per panicle and the number of secondary grains per panicle across all tillers (mainstem, tiller 1, tiller 2) from all seed rates. Each point on the graph represents the average of one type of tiller from one replicate at one seed rate. 5

Field Crops Research 242 (2019) 107592

J. Finnan, et al.

Fig. 2. The effect of seed rate on primary grain weight (a) and on secondary grain weight (b) on each whorl of the mainstem panicle and average grain weight per mainstem panicle. Results represent averages over two years, 2016 and 2017. Error bars represent standard error.

grain weight ratio across the whole panicle and on whorl 2 but not on any other whorl, the 2017 ratio was significantly greater than the 2016 ratio. There were no significant interactions between tiller order and year. The relationship between average primary grain weight and average secondary grain weight per panicle for all tillers from each seed rate treatment is shown in Fig. 4. The relationship between primary and secondary grain weight in both years was highly significant. The relationship was unaffected by seed rate or by tiller order.

number of grains per plant had two components, number of grains from mainstem and from tillers (Fig. 5b). Stability of green leaf area per grain (Fig. 5c) was associated with the plasticity of green leaf area per plant, changes in grain numbers were matched by changes in leaf area. Changes in green leaf area per mainstem and in tillers contributed to the plasticity of green leaf area per plant. 4. Discussion Plant phenotypes result from a series of successive processes of organ initiation, differentiation, resource capture, senescence, recycling and reproduction (Kumar et al., 2016). Phenotypic plasticity in plants is a major mechanism to achieve yield stability in variable environments and plasticity extends across a remarkable array of traits including morphology, physiology, anatomy and phenology (Sultan, 2000; Kumar et al., 2017). Adjustments to the number and sizes of sinks is mediated by signal sensing/transmission mechanisms which convey information on the availability of resources within the plant (Kumar et al., 2016). Sugars play a pivotal role as signalling molecules together with plant hormones (Sultan, 2000; Rolland et al., 2006). The sensing of such signals by apical and secondary meristems together with storage tissues

3.3. The contribution of plasticity to trait stability The difference in yield between the seed rate treatments used for sampling in this study were previously found to be small (Finnan et al., 2018) due to the ability of oat crops to compensate for low plant populations. Yields from the seed rate treatments used for sampling in this study were highly correlated with the number of grains per square meter (R2 = 0.76; P < 0.001), the stability of yield and grain numbers over a wide range of seed rates (and their corresponding plant populations) is shown in Fig. 5a. Grain number stability was associated with plasticity in the number of grains per plant. The plasticity of the 6

Field Crops Research 242 (2019) 107592

J. Finnan, et al.

Fig. 3. The effect of tiller order in the 100 seeds/m2 treatment on primary grain weight (a) and on secondary grain weight (b) on each whorl of the panicle and on average grain weight per panicle. Results represent averages over two years, 2016 and 2017. Error bars represent standard error.

of winter wheat grown at a plant density of 100 plants/m2 contained between 50 and 60 grains per ear illustrating the plasticity of the oat panicle in comparison to the inflorescences of wheat and barley. Wheat spikelets contain higher grain numbers than spikelets of oats (PeltonenSainio and Peltonen, 1995) yet maximum spikelet numbers per ear are substantially lower in wheat compared to oats. Rawson (1971) found that the number of spikelets per ear in wheat could not be increased beyond 25. Darwinkel (1978) found a similar number of spikelets on mainstem wheat ears at a plant population of 100 plants/m2 and found that there was only a slight increase in the number of spikelets per ear at a plant population of 5 plants/m2. In contrast, oat mainstem spikelet numbers in this study exceeded 100. Rice panicles have also been shown to exhibit high plasticity (Adriani et al., 2016; Dingkuhn et al., 2015). In terms of plasticity, oat panicles have more in common with the panicles of rice than with the ears of wheat and barley. Spikelet number can be influenced by the rate of spikelet initiation, the duration of spikelet initiation and spikelet mortality (Hay and Walker, 1989). Kirby and Faris (1970) reported that the duration of spikelet initiation in barley was more sensitive to seed rate than the rate of spikelet initiation and higher spikelet numbers in wheat have been related to a longer period between floral initiation and terminal spikelet

generates morphological plasticity in the form of sinks of various sizes (Kumar et al., 2016). The shape and size of sinks is the result of interactions between the sets of genes governing specific meristems on the one hand and competition for acquired resources on the other hand (Dingkuhn et al., 2005). Models have been developed based on these principles which can successfully predict phenotypic plasticity for genotypes grown in different environments (Dingkuhn et al., 2005; Luquet et al., 2006). Mainstem oat panicles exhibited high plasticity as seed rate was changed, grain numbers per mainstem panicle in the lowest seed rate treatment were more than twice that in the highest seed rate treatment. Oat panicles exhibit greater plasticity than wheat spikes (Rajala and Peltonen-Sainio, 2011), Peltonen-Sainio and Peltonen (1995) reported a 3–4 fold increase in spikelet and grain numbers on mainstem oat panicles under different nitrogen treatments. It is possible that the full extent of the plasticity of the oat panicle was not explored within the seed rate range used in this study. For example, higher grain number per panicle may occur at seed rate treatments below 100 seeds/m2 but such seed rates may not be agronomically relevant. Mainstem panicles in the lowest seed rate treatment (100 seeds/m2) contained an average of 200 grains. In contrast, Darwinkel (1978) found that mainstem ears 7

Field Crops Research 242 (2019) 107592

J. Finnan, et al.

A two and a half fold increase in grain numbers per mainstem panicle was accompanied by a two fold increase in green leaf area per mainstem as seed rate decreased from 500 seeds/m2 to 100 seeds/m2. Changes in the number of leaves with green leaf material together with changes in leaf length and leaf width contributed to the increase in green leaf area and, both effects contributed to the stability of the leaf area per grain. Increase in green area per stem in winter wheat with decreasing plant density was attributed to longer leaves and not to changes in the number of leaves per stem (Whaley et al., 2000). Similarly, increases in leaf length and width with decreasing plant density have been reported in barley (Kirby and Faris, 1970). Increases in green leaf number with reducing plant density have been reported in both barley (Kirby and Faris, 1972) and wheat (Puckridge and Donald, 1967) and may be caused by changes in leaf initiation, the rate or duration of leaf expansion or to changes in the rate of leaf senescence (Hay and Walker, 1989). An increase in green leaf area with increasing tiller order was due, primarily, to an increase in green leaf numbers per stem which may reflect the later development of tillers and the fact that their lower leaves had not senesced to the same extent as mainstem leaves. At plant level, the ratio between green leaf area and grain numbers was shown to be a conservative characteristic across a wide range of seed rates. The plasticities of grain numbers per plant and of green leaf area per plant were closely matched ensuring that the quantity of green leaf area per grain remained stable. Differences in radiation interception between these seed rate treatments were found to be small (Finnan et al., 2018). In this study, we have shown that oat plants at low plant densities increase solar radiation interception through greater number of larger leaves, possibly attributable to increased nitrogen uptake per plant. Grain weight is the most stable of all yield components (Gales, 1983; Peltonen-Sainio et al., 2007; Sadras and Slafer, 2012; Slafer et al., 2014) yet this comparison is relative as changes in grain weight do occur between seasons (Finnan et al., 2018;2019), between treatments (Darwinkel, 1978) and between different plant parts (McLaren, 1981). Seed rate had no significant effect on thousand grain weight in the trials used for sampling in this study (Finnan et al., 2018). Guitard et al. (1961) also reported no effect of seed rate on grain weight in oats although other studies have reported decreases in grain weight with increasing seed rate (Peltonen-Sainio, 1997; Wade and Maunsell, 2004). The principal source of variation in grain weight in our study was grain type (primary vs secondary) followed by whorl position. Such variation has been well documented in many studies (Youngs and Shands, 1974; Doehlert et al., 2002; Rajala and Peltonen-Sainio, 2011; White and Finnan, 2017). The potential weight of secondary grains appears to be restricted which may result from lower endosperm cell numbers, later differentiation and pollination may also delay the start of grain filling (Tibelius and Klinck, 1987). Differences in grain weight between whorls have been attributed to differences in vascular transport capacity as whorls at the bottom of the panicle have greater assimilate demand than whorls at the top of the panicle (Housley and Peterson, 1982) or to earlier differentiation and pollination of grains at the top of the panicle (Rajala and Peltonen-Sainio, 2004). Increases in grain weight between the bottom and top whorls of the panicle were greater for secondary grains (> 40%) than for primary grains (< 20%), this effect may have been caused by greater competition for assimilate in the whorls at the bottom of the panicle. Many studies have reported that grain weight declines with increasing tiller order (Cannell, 1969; McLaren, 1981; Darwinkel, 1978). However, we found little difference between individual grain weights on the mainstem and the second tiller while grain weights on the first tiller were higher than on the mainstem and second tiller. Higher primary and secondary grain weights on the first tiller possibly result from a more favourable source/sink balance on this shoot as leaf area per grain increased with increasing tiller order and higher ratios of leaf area per grain could potentially favour grain filling resulting in higher grain weights. However, the weight of both primary and secondary grains on

Fig. 4. The relationship between the average primary grain weight per panicle and the average secondary grain weight per panicle across all tillers (mainstem, tiller 1, tiller 2) from three seed rates (100 seeds/m2, 300 seeds/m2, 500 seeds/ m2). Each point on the graph represents the average of one type of tiller from one replicate at one seed rate.

(Rawson, 1970). Reducing the time period of the early and late reproductive phases has been found to result in reduced spikelet numbers in the ears of both wheat and barley (Miralles et al., 2000). The late reproductive phase from terminal spikelet to anthesis has been identified as a critical phase in the determination of the number of fertile grains at anthesis (Fischer, 1985) and increased duration of this phase has been related to increased floret survival in cereals (Miralles et al., 2000). In oats, the number of grains per panicle has been found to be related to the length of the period of maximum floret production (Peltonen-Sainio, 1994, 1999) while floret set in oats has been found to decrease with decreased duration of the pre-anthesis phase (PeltonenSainio and Peltonen, 1995). A decrease in the period of maximum floret production with increasing tiller order explains the decrease in grain numbers per panicle with increasing tiller order, the duration of the period of spikelet initiation becomes shorter with delayed tiller emergence so the number of spikelets per ear declines progressively with increasing tiller order (Darwinkel, 1980; Hay and Walker, 1989). All panicles, irrespective of size, displayed a gradient in plasticity from the base to the top of the panicle. This gradient was also observed when different levels of nitrogen were applied to winter oats when the greatest changes in spikelet numbers occurred in the whorls at the base of the panicle (White and Finnan, 2017). Spikelet differentiation begins at the top of the panicle, proceeding towards the bottom of the panicle over a period of 18 days (Bonnett, 1961), the greater plasticity of the whorls at the bottom of the panicle may reflect resource availability towards the end of the period of spikelet differentiation. The ratio of primary to secondary grain numbers was shown to be a very conservative characteristic across panicles from all seed rates and tillers, changes in grain numbers per panicle was very closely related to changes in spikelet numbers. Similarly, Peltonen-Sainio and Peltonen (1995) reported substantial increases in the number of spikelets per panicle but not in the number of grains per spikelet after nitrogen fertilization. White and Finnan (2017) found that the ratio of primary to secondary grains did not change with tiller order when plants had sufficient nitrogen although nitrogen could improve the fertility of secondary grains. In our study, minor changes in the ratio of primary to secondary grain numbers between the years may relate either to conditions during floret initiation or to conditions during the period immediately prior to anthesis, a period which has been identified as critical to final grain number determination (Finnan et al., 2019). Thus, stressful conditions caused by biotic or abiotic stress during these periods may alter the ratio of primary to secondary grains by causing some abortion of secondary grains. 8

Field Crops Research 242 (2019) 107592

J. Finnan, et al.

Fig. 5. Stability of yield, grain numbers and green leaf area per grain in relationship to the plasticity of grain numbers per plant and green leaf area per plant at the spring plant populations corresponding to the seed rate treatments in this study. The relationship between yield and grain numbers is shown in Fig. 5a (data from Finnan et al., 2018).The relationship between grain numbers per square area (stable parameter) and grain numbers per plant (plastic parameter) is shown in Fig. 5b. The relationship between green leaf area per grain (stable parameter) and green leaf area per plant (plastic parameter) is shown in Fig. 5c (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).

9

Field Crops Research 242 (2019) 107592

J. Finnan, et al.

the first tiller increased by approximately 2 mg in comparison to grain weights on other tillers, this increase represents less than 10% of mainstem grain weight variation. Consequently, grain weight variation between tillers was less than intrapanicle grain weight variation. Grains from the first tiller made up approximately 30% of total grain numbers in the lowest seed rate treatment yet the thousand grain weight of this treatment did not differ significantly from the thousand grain weight of the other seed rate treatments in this study (Finnan et al., 2018) further suggesting that grain weight variation between tillers was insufficient to significantly alter the thousand grain weight of the grain population from the lower seed rate treatments. In this study, grain weight remained stable in spite of large changes in the number of grains per panicle suggesting that grain fill was not limited by assimilate supply across a wide range of plant densities. Furthermore, the stability of the relationships between primary and secondary grain numbers and grain weight across a wide range of panicle sizes act to preserve the stability of the grain population. The stability of certain traits is attributable, at least in part, to the plasticity of other traits (Bradshaw, 1965; Sadras, 2007). In this study, stability of yield (and grains numbers) across a wide range of seed rates was associated with plasticity in grain numbers per plant. This is true for all cereals but in oats this plasticity is related both to the plasticity of the mainstem panicle as well as the ability of the plant to produce tillers at low plant densities. The variety used in this study exhibited high mainstem plasticity and only produced tillers at low plant populations but this balance may change in other oat varieties. Similarly, stability of individual grain weight is associated with the stability of green leaf area per grain which, in turn, is associated with the plasticity of leaf area per stem and leaf area per plant. The capacity of individual genotypes and species to express different phenotypes in different environments, phenotypic plasticity, is highly significant as plasticity determines adaptation to resource availability and stress. More research is needed to understand plasticity in the oat plant in different environments and when subjected to stress. Crop models which simulate phenotypic plasticity have been used to predict the phenotypic plasticity of traits which contribute to yield in rice. Such models could also be used to develop and test our understanding of the plasticity of important traits in oats and could also be used to develop ideotypes best suited to adapt to our changing environments.

Bonnett, O.T., 1961. The Oat Plant: Its Histology and Development. Bulletin/University of Illinois (Urbana-Champaign campus) Agricultural Experiment Station; no. 672. Bradshaw, A.D., 1965. Evolutionary significance of phenotypic plasticity in plants. Adv. Genetics 13, 115–155 Academic Press. Cannell, R.Q., 1969. The tillering pattern in barley varieties: I. Production, survival and contribution to yield by component tillers. J. Agric. Sci. 72 (3), 405–422. Clemens, R., van Klinken, B.J.W., 2014. The future of oats in the food and health continuum. . British J. Nut 112 (S2), S75–S79. Conry, M.J., Hegarty, A., 1992. Effect of sowing date and seed rate on the grain yield and protein content of winter barley. J. Agric. Sci. 118 (3), 279–287. Darwinkel, A., 1978. Patterns of tillering and grain production of winter wheat at a wide range of plant densities. Neth. J. Agric. Sci. 26, 383–398. Darwinkel, A., 1980. Ear development and formation of grain yield in winter wheat. Neth. J. Agric. Sci. 28 (3), 156–163. Dingkuhn, M., Luquet, D., Quilot, B., De Reffye, P., 2005. Environmental and genetic control of morphogenesis in crops: towards models simulating phenotypic plasticity. Aust.J. Agric. Res. 56 (11), 1289–1302. Dingkuhn, M., Laza, M.R.C., Kumar, U., Mendez, K.S., Collard, B., Jagadish, K., Singh, R.K., Padolina, T., Malabayabas, M., Torres, E., Rebolledo, M.C., 2015. Improving yield potential of tropical rice: achieved levels and perspectives through improved ideotypes. Field Crops Res. 182, 43–59. Doehlert, D.C., McMullen, M.S., Riveland, N.R., 2002. Sources of variation in oat kernel size. Cereal Chem. 79 (4), 528–534. Finnan, J.M., Hyland, L., Burke, B., 2018. The effect of seed rate on radiation interception, grain yield and grain quality of autumn sown oats. Eur. J. Agron. 101, 239–247. Finnan, J., Burke, B., Spink, J., 2019. The effect of nitrogen timing and rate on radiation interception, grain yield and grain quality in autumn sown oats. Field Crops Res. 231, 130–140. Fischer, R.A., 1985. Number of kernels in wheat crops and the influence of solar radiation and temperature. J. Agric. Sci. 105 (2), 447–461. Gales, K., 1983. Yield variation of wheat and barley in Britain in relation to crop growth and soil conditions—a review. J. Sci. Food Agric. 34 (10), 1085–1104. Gallagher, J.N., Biscoe, P.V., Scott, R.K., 1975. Barley and its environment. V. Stability of grain weight. J. App. Ecol 12 (1), 319–336. Grafius, J.E., 1978. Multiple characters and correlated response 1. Crop Sci. 18 (6), 931–934. Guitard, A.A., Newman, J.A., Hoyt, P.B., 1961. The influence of seed rate on the yield and the yield components of wheat, oats and barley. Can. J. Plant Sci. 41 (4), 751–758. Hay, R.K., Walker, A.J., 1989. Introduction to the physiology of crop yield. Longman Group UK Limited. Housley, T.L., Peterson, D.M., 1982. Oat stem vascular size in relation to kernel number and weight. I. Controlled environment 1. Crop Sci. 22 (2), 259–263. Jones, I.T., Hayes, J.D., 1967. The effect of Seed rate and growing season on four oat cultivars: I. Grain Yield and its Components. J. Agric. Sci. 69 (1), 103–109. Kirby, E.J.M., Faris, D.G., 1970. Plant population induced growth correlations in the barley plant main shoot and possible hormonal mechanisms. J. Exp. Bot. 21 (3), 787–798. Kirby, E.J.M., Faris, D.G., 1972. The effect of plant density on tiller growth and morphology in barley. J. Agric. Sci. 78 (2), 281–288. Kumar, U., Laza, M.R., Soulié, J.C., Pasco, R., Mendez, K.V., Dingkuhn, M., 2016. Compensatory phenotypic plasticity in irrigated rice: sequential formation of yield components and simulation with SAMARA model. Field Crops Res. 193, 164–177. Kumar, U., Laza, M.R., Soulié, J.C., Pasco, R., Mendez, K.V., Dingkuhn, M., 2017. Analysis and simulation of phenotypic plasticity for traits contributing to yield potential in twelve rice genotypes. Field Crops Res. 202, 94–107. Luquet, D., Dingkuhn, M., Kim, H., Tambour, L., Clement-Vidal, A., 2006. EcoMeristem, a model of morphogenesis and competition among sinks in rice. 1. Concept, validation and sensitivity analysis. Func.Plant Biol. 33 (4), 309–323. McLaren, J.S., 1981. Field studies on the growth and development of winter wheat. J. Agric. Sci. 97 (3), 685–697. Mahadevan, M., Calderini, D.F., Zwer, P.K., Sadras, V.O., 2016. The critical period for yield determination in oat (Avena sativa L.). Field Crops Res. 199, 109–116. Miralles, D.J., Richards, R.A., Slafer, G.A., 2000. Duration of the stem elongation period influences the number of fertile florets in wheat and barley. Funct. Plant Biol. 27 (10), 931–940. Peltonen-Sainio, P., 1990. Morphological and physiological characters behind highyielding ability of oats (Avena sativa), and their implications for breeding. Field Crops Res. 25 (3–4), 247–252. Peltonen-Sainio, P., 1994. Growth duration and above-ground dry-matter partitioning in oats. Agric. Food Sci. 3 (2), 195–198. Peltonen‐Sainio, P., Järvinen, P., 1994. Effects of seed rate on growth duration and accumulation and partitioning of dry matter in oats. J. Agron. Crop Sci. 173 (3–4), 145–159. Peltonen-Sainio, P., Peltonen, J., 1995. Floret set and abortion in oat and wheat under high and low nitrogen regimes. Eur. J. Agron. 4 (2), 253–262. Peltonen-Sainio, P., 1997. Groat yield and plant stand structure of naked and hulled oat under different nitrogen fertilizer and seed rates. Agron. J. 89 (1), 140–147. Peltonen-Sainio, P., 1999. Growth and development of oat with special reference to source-sink interaction and productivity. Crop Yield. Springer, Berlin, Heidelberg, pp. 39–66. Peltonen-Sainio, P., Kangas, A., Salo, Y., Jauhiainen, L., 2007. Grain number dominates grain weight in temperate cereal yield determination: evidence based on 30 years of multi-location trials. Field Crops Res. 100 (2–3), 179–188. Peltonen-Sainio, P., Jauhiainen, L., Sadras, V.O., 2011. Phenotypic plasticity of yield and agronomic traits in cereals and rapeseed at high latitudes. Field Crops Res. 124 (2), 261–269.

5. Conclusions The plasticity of the oat panicle offers a compensatory mechanism by which grain numbers can be buffered across a wide range of environmental and agronomic conditions. Grain weight stability is preserved across a wide range of panicle sizes by changes in green leaf area per stem with panicle size and by the stability of the relationship between primary and secondary grain numbers. Acknowledgements The authors are deeply grateful for the assistance of Peter Gaskin, Frank Ryan, Kevin Murphy, Mickael Hardy, Vincent Robert, Cathal Doran, Guillaume Fremont, Florian Clement, Mickael Caudron, Louelli Koffi, Thibault Desmons and Joshua Laycock. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.fcr.2019.107592. References Adriani, D.E., Dingkuhn, M., Dardou, A., Adam, H., Luquet, D., Lafarge, T., 2016. Rice panicle plasticity in near Isogenic Lines carrying a QTL for larger panicle is genotype and environment dependent. Rice 9 (1), 28.

10

Field Crops Research 242 (2019) 107592

J. Finnan, et al. Power, J.F., Alessi, J., 1978. Tiller development and yield of standard and semidwarf spring wheat varieties as affected by nitrogen fertilizer. J. Agric. Sci. 90 (1), 97–108. Puckridge, D.W., Donald, C.M., 1967. Competition among wheat plants sown at a wide range of densities. Aust. J. Agric. Res. 18 (2), 193–211. Rajala, A., Peltonen-Sainio, P., 2004. Intra-plant variation for progress of cell division in developing oat grains: a preliminary study. Agric. Food Sci. 13, 163–169. Rajala, A., Peltonen-Sainio, P., 2011. Pollination dynamics, grain weight and grain cell number within the inflorescence and spikelet in oat and wheat. Agric. Sciences 2 (03), 283–290. Rawson, H.M., 1970. Spikelet number, its control and relation to yield per ear in wheat. Aust. J. Biol. Sci. 23 (1), 1–16. Rawson, H.M., 1971. An upper limit for spikelet number per ear in wheat as controlled by photoperiod. Aust. J. Agric. Res. 22 (4), 537–546. Rolland, F., Baena-Gonzalez, E., Sheen, J., 2006. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675–709. Ryan, P.M., London, L.E., Bjorndahl, T.C., Mandal, R., Murphy, K., Fitzgerald, G.F., Shanahan, F., Ross, R.P., Wishart, D.S., Caplice, N.M., Stanton, C., 2017. Microbiome and metabolome modifying effects of several cardiovascular disease interventions in apo-E−/− mice. Microbiome 5 (1), 30. Sadras, V.O., 2007. Evolutionary aspects of the trade-off between seed size and number in crops. Field Crops Res. 100 (2–3), 125–138. Sadras, V.O., Slafer, G.A., 2012. Environmental modulation of yield components in cereals: heritabilities reveal a hierarchy of phenotypic plasticities. Field Crops Res. 127, 215–224. SAS, 2014. Version 9.4. SAS Institute Incorporated, Cary North Carolina, USA. Slafer, G.A., Savin, R., Sadras, V.O., 2014. Coarse and fine regulation of wheat yield

components in response to genotype and environment. Field Crops Res. 157, 71–83. Spink, J.H., Semere, T., Sparkes, D.L., Whaley, J.M., Foulkes, M.J., Clare, R.W., Scott, R.K., 2000. Effect of sowing date on the optimum plant density of winter wheat. Ann. Appl. Biol. 137 (2), 179–188. Sultan, S.E., 2000. Phenotypic plasticity for plant development, function and life history. Trends Plant Sci. 5 (12), 537–542. Thies, F., Masson, L.F., Boffetta, P., Kris-Etherton, P., 2014. Oats and bowel disease: a systematic literature review. Brit. J. Nut 112 (S2), S31–S43. Tibelius, A.C., Klinck, H.R., 1987. Effects of artificial reduction in panicle size on weight of secondary seeds in oats (Avena sativa L.). Can. J. Plant Sci. 67 (3), 621–628. U.S. Food and Drug Administration, 1997. FDA final rule for federal labeling: health claims; oats and coronary heart disease. Fed. Regist. 62, 3584–3681. Wade, A., Maunsell, C., 2004. Assessing the Impact of Improved Crop Management on Naked Oat Quality for Poultry Production Part of Avian Feed Efficiency From Naked Oats (AFENO). HGCA Project Report 337. https://cereals.ahdb.org.uk/publications/ 2004/may/13/assessing-the-impact-of-improved-crop-management-on-naked-oatquality-for-poultry-production.aspx (Accessed 21/12/2018). . Whaley, J.M., Sparkes, D.L., Foulkes, M.J., Spink, J.H., Semere, T., Scott, R.K., 2000. The physiological response of winter wheat to reductions in plant density. Ann. Appl. Biol. 137 (2), 165–177. White, E., Finnan, J., 2017. Crop structure in winter oats and the effect of nitrogen on quality-related characters. J. Crop Improvement 31 (6), 758–779. Youngs, V.L., Shands, H.L., 1974. Variation in oat kernel characteristics within the panicle 1. Crop Sci. 14 (4), 578–580. Zadoks, J.C., Chang, T.T., Konzak, C.F., 1974. A decimal code for the growth stages of cereals. Weed Res. 14 (6), 415–421.

11