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Secondary traits for maize grain yield under drought stress conditions

1         Importance of secondary traits of maize under drought stress

Drought can affect maize production by decreasing plant stand during the seedling stage, by decreasing leaf area development and photosynthesis rate during the pre-flowering period, by decreasing ear and kernel set during flowering, and by decreasing photosynthesis and inducing early leaf senescence during grain-filling. Additional reductions in production may come from an increased energy and nutrient consumption of drought adaptive responses, such as increased root growth under drought (Bänziger et al., 2000).

Two important physiological processes appear to be involved in the increase of drought tolerance in maize: 1) sustained leaf photosynthesis during grain filling, which contributes to increases in dry matter accumulation and an 2) increase in kernel number due to higher partitioning to the kernels during the sensitive period of kernel number determination (Araus et al., 2008).

Secondary traits are used for selecting maize under drought stress, because the selection based on grain yield alone is inefficient due to a decline in heritability under stress (Bolanos et al., 1996; Monneveux et al., 2008).

Requirements for a novel secondary trait: To be effective, secondary traits should be genetically associated with grain yield under drought in the target environment, genetically variable, highly heritable, easy to measure, and stable over time (Blum, 1988; Campos et al., 2004; Monneveux et al., 2008). The heritability of the secondary trait should be higher under stress indicating that the trait is less affected by the environment (Araus et al., 2008). Additionally it is important that the selective traits are not associated with poor yields under unstressed conditions and are related to productivity rather than survival mechanisms. Furthermore, the measurement of the secondary trait should be cheaper than the measurement of grain yield.

Monneveux et al. (2008) came to the conclusion that some long established secondary traits (i.e. anthesis-silking interval) have become less important, while others have become more relevant. To counteract the steady reduction in genetic gain over time it is necessary to identify alternative traits or novel strategies.

2    Traits measured during flowering and grain filling

Anthesis Silking Interval (ASI)
Maize is more sensitive than other cereals to water deficits and high temperatures at flowering because anthers and silks are separated by about 1 m, and pollen and stigmas are exposed to the environment (Bolaños and Edmeades, 1993; Monneveux et al., 2008). The period in which maize is particularly sensitive to water stress is 1 week before to 2 weeks after flowering (Edmeades et al., 1999; Campos et al., 2004). When photosynthesis at flowering is reduced by drought, silk growth is delayed, leading to an increase the anthesis-silking interval (ASI). Due to the delay of silk emergence, the reduction of pollen viability, the number of kernels fertilized per ear is reduced (Bolaños and Edmeades, 1993).

Tassel size
The shape of the tassel affects the quantity of radiation reaching the canopy, thereby affecting leaf photosynthesis and the partitioning of assimilate towards the developing grain. Tassel dry weight and ear dry weight were shown to be negatively correlated, indicating an association between reduced tassel size and improved partitioning toward the ear. Further, detasselling can lead to an important increase of yield under drought conditions (Monneveux et al., 2008). Thus, tassel size, tassel branch number as well as tassel dry weight seem to be promising traits for selecting drought tolerant genotypes. The selection for smaller tassel size is limited by quantity of pollen needed to ensure fertilization. An alternative approach could be to grow cms maize hybrids with a pollen donor (plus hybrid system). Within this system pollen dispersal has to be ensured.

3    Photosynthesis/ Radiation uptake and radiation use efficiency
Grain yield can be defined as the product of incident radiation received per day during the growing season (RAD), intercepted radiation over crop (%RI), green leaf duration (GLD), radiation use efficiency (RUE) and harvest index (HI), where the first three factors influence biomass development (Araus et al., 2008).

GY = RAD x %RI x RUE x HI
As the developing maize ear has very little capacity to mobilize and attract the plant reserves stored in the stem its first two weeks of life (Bänziger et al., 2000) a higher radiation uptake and radiation use efficiency should lead to an increase availability of sugars for transportation during flowering and grain filling leading to higher grain yield (Araus et al., 2008). The radiation use efficiency is influenced by the chlorophyll content and the efficiency of photosystem II.

3.1    Chlorophyll content
The potential of taking up radiation and the ability of a leaf to stay green during stress can be assessed indirectly by measuring the chlorophyll content (Araus et al., 2008). The chlorophyll content can be analyzed in the lab but also be measured in the field with a SPAD meter. The SPAD meter SPAD-502 calculates the ratio of absorbance at 650 nm (chlorophyll absorbance peak) and at 940 nm (non-chlorophyll absorbance). The optimization of crop photosynthesis under stress requires a balance between maximizing assimilation at critical growth stages and avoiding the destructive effects of excess radiation (Araus, 2002). As such the relationship of chlorophyll content and grain yield in maize can be 1) positive due to increased production and transport of energy from photosynthesis or negative due to remobilization of energy from chlorophyll. Bolaños and Edmeades (1993) found no differences among cultivars in rate of leaf senescence, as measured by chlorophyll concentration during the last half of grain-filling. This result was consistent with visual scores of rates of leaf senescence.

3.2    Efficiency of photosystem II
The radiation use efficiency can be assessed by measuring the efficiency of the photosystem II (ΦPSII). ΦPSII can give a measure of the rate of linear electron transport and an indication of overall photosynthesis. If ΦPSII is <0.8, this indicates that PSII is damaged due to photo inhibition. Fracheboud et al., (1999) came to the conclusion that ΦPSII can be used to estimate photosynthesis accurately in a wide range of environmental conditions and can be used as selection tool for cold tolerance of photosynthesis in maize. For the measurement of ΦPSII in the field a portable fluorometer can be used (ADC OS5p Advanced Modulated Fluorometer, LI6400-40 Leaf Chamber Fluorometer, Z990 FluorPen).

3.3    Chlorophyll fluorescence
If the light is not intercepted by the photosynthetic system the excess energy is emitted by chlorophyll fluorescence. The chlorophyll fluorescence increases with drought stress. The dissipation of excess energy as fluorescence can be measured by a pulse-amplitude modulated (PAM) fluorometer. In general the chlorophyll content, efficiency of the photosystem II and the chlorophyll fluorescence vary along the leaf and within leaves (Lichtenthaler et al., 2005). As such it is difficult to a) assess a representative value for each genotype and b) to assess drought stress effects on the listed traits. Thus, it is advised to combine the measurement of chlorophyll measurements with an imaging technique (Lichtenthaler et al., 2005) or with the measurement of gas exchange (Maxwell and Johnson, 2000). As portable fluorometer the Licor 6400XT and the PAM 2500 can be used.

Selmani and Wassom (1993) found no significant correlation between fluorescence and maize grain yield under drought. The authors concluded that grain yield does not depend solely on maintenance of high photosynthesis rates under droughty conditions, but rather on the availability of sink, the translocation of photosynthates, the synchronization of male and female flowering, the leaf area index and duration.

4    Spectral reflectance
Leaf pigments absorb light strongly in the photosynthetic active radiation region (PAR, 400-700 nm) but not in the near infrared region (NIR), thus reducing the reflection of PAR but not of NIR (700-1200 nm) (Araus, 2002). Such a pattern of pigment absorption determines the characteristic reflectance signature of leaves. While leaf reflectance is driven by the chemical composition of the leaves, the reflectance of a canopy is influenced by its geometry as well as the reflectance of single leaves (Linke et al., 2008). The reflectance is used to calculate different reflectance indices, which sum up the large amount of information contained in a reflectance spectrum. Some of them are related to plant biomass, photosynthetic size and radiation use efficiency. Other parameters are related to the physiological status, e.g. water content.

Weber et al. (2012) reported, that spectral reflectance measures on leaf and canopy level could explain at maximum 40% of grain yield under drought and well watered conditions.

Several spectral reflectance indicies were developed to measure plant biomass, plant water content and photosynthesis (see article on spectral reflectance indices).

5    Water uptake, water use efficiency and water status

Water used by plants is directly associated with dry matter accumulation as water vapour and carbon dioxide pass through the stomata. Grain yield can be defined as the product of water transpired by the crop (W), the water use efficiency (WUE) and the harvest index (HI):

GY = W * WUE * HI
5.1    Water uptake
With the stem heat balance method the mass flow rate in the stem can be measured with a constant or variable heating power. The relocation of the heat impulse is measured above the heating source with a sensor. It is possible to measure weekly sap flow rates of corn with gauges with around 10% standard deviation and 80-95 confidence, but not at transpiration rates >100 mm/S (Cohen et al., 1993). The disadvantage is that lots of gauges are needed per plot to measure a plot mean value.

5.2    Transpiration and stomatal conductance
The potential amount of water transpired by a crop is the sum of the precipitation during the growing season and the available water stored in the soil. Leaf conductance is determined by the degree which stomata are open, and this parameter depends on the water status and the evaporative demand of the plant (Araus et al., 2008).
As the stomata influence the influx of CO2, the closure of the stomata leads to a CO2 shortage. As a result not the total photosynthetic capacity is used, which leads to a reduced photosynthetic N use efficiency. On the other hand if photosynthesis is carried on water is lost. Consequently the usefulness of reduced stomatal conductance depends upon the trade of between loss of production and the need to prevent dehydration. Thus, water saving genotypes, which have an optimal balance between transpiration and stomatal conductance, are of interest.

The stomatal conductance can be measured with a porometer. With high specific leaf area the transpiration rate increases. As such it is necessary to assess leaf area in parallel. In general, the stomata closure under stress is patchy. Thus, different sections of a leaf should be measured. Additionally, stomatal conductance varies diurnally (Jones, 2007). The short-term changes can be substantially larger than treatment differences.

5.3    Leaf/ canopy temperature
When stomata close, transpiration is reduced and the cooling effect is reduced leading to leaf and canopy temperature increases (Selmani and Wassom, 1993). Thus canopy and leaf temperature can serve as an indirect measure of plant transpiration and plant water status (Bolaños and Edmeades, 1993). Lower leaf or canopy temperatures indicate enhanced capacity to take up soil moisture or to maintain a better plant water status (Araus et al., 2008). Canopy temperature is affected by the relative amount of desiccated and dead leaves in the canopy so canopy temperature is related to leaf death score.

Transpiration driven canopy temperature depression (CDT) can be measured using an infrared thermometer. Canopies emit long-waved infrared radiation as a function of their temperature. The infrared thermometer senses this radiation and converts it to an electrical signal which is displayed as temperature (Stefan-Boltzmann blackbody law, Planck’s law). During measurement, the position (distance, angle) must be maintained the same. Cloudy or windy conditions should be avoided. Additionally the readings should be made with the sun at the back of the operator around noon. A significant negative correlation between maize grain yield and canopy temperature under water-stressed conditions was reported, indicating that lines which maintained low temperatures produced higher yields (Selmani and Wassom, 1993).

5.4    Leaf rolling
The initiation of leaf rolling is associated with higher leaf temperature, lower leaf water potential and osmotic adjustment. Leaf rolling is an indication of leaf water status and may identify plants with inadequacies in water uptake or turgor maintenance (Edmeades et al., 1999). Leaf rolling has a negative effect of yield as it reflects hydraulic conductance and it reduces the quantity of light intercepted by the canopy.

Leaf rolling can be measured by using a visual scale from 1 to 5, where 1 is low and 5 severe leaf rolling (Bänziger et al. 2000).

Bolaños and Edmeades (1993) could not establish any association between leaf rolling score and either pre-swan leaf water potential or changes in leaf water status. Because it is a survival trait it has little influence on yield components. Thus, leaf senescence and leaf rolling can be useful as secondary traits in a preliminary selection among largely drought susceptible germplasm but they become less informative as the level of drought tolerance improves.

5.5    Senescence and stay green
Water stress accelerates the senescence of lower leaves in maize (Bolaños and Edmeades, 1993). Delayed leaf senescence could diminish evaporation while increasing water use and water use efficiency. Further, stay green plants are characterized by a post-flowering drought resistance phenotype that gives plants resistance to premature senescence (Cattivelli et al., 2008).
Genotypic variation in delayed onset and reduced rate of leaf senescence can be explained by differences in specific leaf nitrogen and N uptake during grain filling. As such senescence is not only indicating drought stress but also plant N status.

The senescence of leaves can be measured by chlorophyll concentration during the last half of grain-filling. Additionally a visual score from 1-100 can be used, where 1 implicates green and 100 senescent plants (Bänziger et al., 2000)(Bänziger et al. 2000).

5.6    Leaf angle
Differences in the rate of dry matter accumulation can be attributed to differences in light interception caused by variability in maximum leaf area index, leaf senescence during grain filling and efficiency of utilization of intercepted radiation as a result of changes in leaf angle (Tollenaar and Lee, 2002; Araus et al., 2008).

Erect leaves should increase water use efficiency, as photosynthesis per unit intercepted radiation increases and mean incident radiation flux per unit leaf surface is reduced (Edmeades et al., 1999).

6    Biomass
While under drought prone conditions genotypes which save water (high water use efficiency) are better suited, as drought conditions are less severe, genotypes able to use more water (regardless of water use efficiency) will yield more (Araus et al., 2008). Water use efficiency may be improved by early vigor, phonological adjustment, increased surface reflectance and decreased residual transpiration as well as enlarged photosynthetic capacity. None of physiological or morphological traits indicative of improved water status correlated with grain yield under drought, although some had relatively high heritability (Bolanos et al., 1996). The lack of direct and correlated changes in traits related to plant water status due to selection suggests the traits are only weakly associated with grain yield under severe moisture stress (Bolaños and Edmeades, 1993). Thus improved drought tolerance might be the result of increased partitioning of biomass to the developing ear rather than change in plant water status.

6.1    Early vigor
Genotypes with early vigor and good seedling establishment shade the soil surface and increase thereby crop transpiration at the expense of soil evaporation. There may also be fewer weeds because a more vigorous crop should prove more competitive (Richards, 2006). Early vigor is influenced by thousand kernel weight and the age of the seed.  Additionally management practices like sowing the seeds at a higher sowing rate, with more nitrogen and reduced depths may improve crop vigor.

The early development can be measured indirectly using a GreenSeeker Device (see also NDVI).

6.2    Root biomass
Maize yield improvement is the result of increased interception of radiation and greater uptake of nutrients and water. Differences in rooting patterns change the amount and timing of water availability to the crop. Greater depth and extend of soil water extraction could increase the amount of water transpired, if this results in the avoidance of water deficits at critical growth stages, it would increase harvest index.

The wide-scale evaluation of root characteristics and root development under field conditions remains impractical, so the development of tagging markers is preferred to manipulate root traits. That’s why most of research is conducted under laboratory conditions and at early developmental stages (Campos et al., 2004). To assess the rooting depth indirectly one can measure the force necessary to remove the plants from the soil. Nevertheless this would damage the soil structure. Alternatively the number of crown roots could be easily accessed visually. Further, measures of water efficiency (see above) could be used as indirect traits for root length.

6.3    Stem biomass
Genotypes with greater plant height are often larger in overall plant size, intercept more light and use water faster by transpiration, leading to lower plant water status, higher leaf death scores and more spikelet sterility. Thus, plant height or respectively stem biomass are negatively related to harvest index (Edmeades et al., 1999). The reduction of plant height to an optimal range could increase yield potential and simultaneously reduce the risk of lodging (Araus et al., 2008). The reduction of plant height could also lead to enhanced partitioning towards the growing ear which in turn might result in increasing number of kernels per ear. The assessment of shoot biomass is very laborious because it has to be harvested, dried and weighted. As a result non-destructive biomass estimations like spectral reflectance indices are useful for continuous shoot biomass estimation during the whole crop cycle (Marti et al., 2007, see also spectral reflectance indices). One of the most widely used SRI is the Normalized Difference Vegetation Index (NDVI) which relates the difference between near infrared reflectance and red wavelength reflectance with the reflectance of both wavelengths. The NDVI is more sensitive to changes in the crop canopy when the leaf area index is low. It becomes saturated when the crop canopy closes.

The development of shoot biomass, yield potential  and leaf area index  of maize could be accurately predicted with NDVI measured with a GreenSeekerTM sensor (GreenSeeker Hand-Held Data Collection and Mapping Unit, NTech Industries, Ukiah, CA, USA).

Grain filling and the mobilization of stem reserves
The harvest index depends on the relative proportion of pre- and postanthesis biomass and on the mobilization of preanthesis assimilates to the grain. An important source of carbon for grain filling is the stem reserve, which is determined by stem length and stem dry weight per unit stem length. The capacity of mobilizing assimilates might depend on the stem length or the stem diameter. The loss of stem weight might be indicated due to a loss in stem diameter. The mobilization of stem reserves can only be useful in environments where terminal drought is the main recurrent problem (Cattivelli et al., 2008).

Stem elongation phase

A longer stem elongation phase might result in greater crop growth during this phase and more grains being filled (Slafer et al. 1996, 2001 in Araus et al. 2008). Extending the duration of stem elongation without changing the timing of anthesis would increase the number of kernels per ear and the harvest index without changing the amount of water utilized (Araus et al. 2002).  Nevertheless it has to be clarified whether extending the duration of grain-filling by selecting for survival is effective to increase translocation of reserves to the grain (Richards et al. 1991).

6.4    Leaf biomass
If radiation is not intercepted by the crop and strikes the ground, evaporation/transpiration ratio will increase. As leaf area influences the cover of the soil it influences the radiation intercepted as well as the fraction of water lost due to evaporation.

For measuring leaf area leaf area meters such as Delta-T (Cambridge, UK) or LiCor (Lincoln, Nebraska, USA) can be used. Additionally photos can be taken to measure the area by using image analysis software. On the other hand it’s cheaper and faster to measure the altitude and the latitude of the leaf to calculate the area, which represents a rectangle. Nevertheless the standard error should be higher with this method.

The fraction of radiation intercepted by the canopy averaged across crop cycle can be increased by selecting genotypes which reach full soil cover early in the growing season (Araus, 2002). Leaf area maintenance would improve yield stability during drought stress due to better radiation interception when water is available.

7    Potential novel secondary traits/ Summarizing Discussion
Progress in breeding for drought tolerance on maize is likely to entail the selection of plants with a reduced leaf area especially in the upper part of the plants, short thick stems, small tassels, erect leaves, delayed senescence, smaller root biomass and a deep root system with little lateral root branching. Robust spikelet and kernel growth at the cell division and expansion-growth phases with good osmotic adjustment to assist in cell retention of water during drought is also of importance. With respect to drought tolerance three breeding targets can be distinguished: drought tolerance at flowering time, drought tolerance during grain filling and yield stability across a range of environments. Final yield is an integral of the growth over the whole season, a trait that influences the ability of the plant to grow during or survive a period of moisture stress may be relatively unimportant in the context of the total life of the crop. For each trait, the genetic variability, repeatability and inheritance has to be known.

Traits indicative of reproductive success (kernel number/plant, ears/plant and ASI) usually explain much more of the variation in grain yield than traits indicative of plant water status and water use efficiency (leaf extension rate, canopy temperature, leaf chlorophyll concentration, leaf erectness, leaf rolling, and leaf senescence) (Bolaños and Edmeades, 1993; Bolanos et al., 1996). Thus, improved drought tolerance is due to increased partitioning of biomass towards the developing ear during a severe drought stress, rather than to a change in plant water status.  Explanations for the lack of direct selection responses in leaf and stem elongation rate, canopy temperature and canopy senescence include a lack of causal association between them and grain yield, and low heritability or limited genetic variability for the trait (Blum, 1988).

8    Literature
Araus, J.L. 2002. Plant Breeding and Drought in C3 Cereals: What Should We Breed For? Annals of Botany 89(7): 925–940.
Araus, J.L., G.A. Slafer, C. Royo, and M.D. Serret. 2008. Breeding for yield potential and stress adaptation in cereals. Critical Reviews in Plant Sciences 27(6): 377–412.
Blum, A. 1988. Plant breeding for stress environments. CRC Press, Boca Raton, FL.
Bolanos, J., G.O.O. Edmeades, and J. Bolaños. 1996. The importance of the anthesis-silking interval in breeding for drought tolerance in tropical maize. Field Crops Research 48(1): 65–80.
Bolaños, J., and G.O. Edmeades. 1993. Eight cycles of selection for drought tolerance in lowland tropical maize. I. Responses in grain yield, biomass, and radiation utilization. Field Crops Research 31(3-4): 233–252.
Bänziger, M., G.O. Edmeades, D. Beck, and M. Bellon. 2000. Breeding for Drought and Nitrogen Stress Tolerance in Maize: From Theory to Practice. CIMMYT, Mexico, D.F.
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Marti, J., J. Bort, G.A. Slafer, and J.L. Araus. 2007. Can wheat yield be assessed by early measurements of Normalized Difference Vegetation Index? Annals of Applied Biology 150(2): 253–257.
Maxwell, K., and G.N. Johnson. 2000. Chlorophyll fluorescence – A practical guide. Journal of experimental botany 51(345): 659–668.
Monneveux, P., C. Sanchez, and A. Tiessen. 2008. Future progress in drought tolerance in maize needs new secondary traits and cross combinations. Journal of Agricultural Science 146(3): 287–300.
Richards, R.A. 2006. Physiological traits used in the breeding of new cultivars for water-scarce environments. Agricultural Water Management 80(1-3 SPEC. ISS.): 197–211.
Selmani, A., and C.E. Wassom. 1993. Daytime chlorophyll fluorescence measurement in field-grown maize and its genetic variability under well-watered and water-stressed conditions. Field Crops Research 31(1-2): 173–184.
Tollenaar, M., and E.A. Lee. 2002. Yield potential , yield stability and stress tolerance in maize. Field Crops Research 75(February): 161–169.
Weber, V.S., J.L. Araus, J.E. Cairns, C. Sanchez, A.E. Melchinger, and E. Orsini. 2012. Prediction of grain yield using reflectance spectra of canopy and leaves in maize plants grown under different water regimes. Field Crops Research 128: 82–90.

December 23rd, 2012
Topic: Crop Science, Plant breeding Tags: None

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