Drought stress and tropical maize: QTLs for leaf greenness, plant senescence, and root capacitance

Abstract

Genetically improved crops with higher water productivity help maintaining and increasing agricultural production in drought-prone areas. Their development involves, as in the case of maize, selection for high grain yield and improved secondary traits. With the objective of better understanding the role and regulation of the morphology of drought adaptation, a recombinant inbred line (RIL) population of tropical maize (Zea mays L.) was evaluated in six field experiments under intermediate (IS) and severe (SS) drought stress at flowering and under well-watered (WW) conditions in Mexico. The analyses per water regime revealed 32 quantitative trait loci (QTLs) for the five measurements of relative content of leaf chlorophyll (CL), 25 for the five visual ratings of plant senescence (SEN), and 11 for the three measurements of electric root capacitance (RCT). Impressive clusters of QTLs were observed on chromosomes 2 (bins 2.03-05), 4 (bin 4.09), and 10 (bins 10.04-05), suggesting that a small number of genes control chlorophyll metabolism and plant senescence. The high CL and low SEN of the drought resistant parent are aspects of its high water productivity resulting from improved constitutive traits. Co-locations of QTLs for CL, SEN and RCT with QTLs for plant height (PHT), the anthesis-silking interval (ASI), and grain yield (GY) were observed in bins 1.06-07, 8.06, and 4.09 but not for the large QTL clusters on chromosomes 2 and 10, suggesting independent genetic control of reproductive traits. Still, the phenotypic data showed that high CL and low SEN were favorable for grain yield production under drought, while delayed SEN was associated with higher grain yield under WW conditions. CL and SEN are suitable to complement selection for drought tolerance in order to sustain future breeding progress.

Introduction

In view of the limited water resources and the ever growing world population it is necessary to further improve the water productivity of crop plants, for example by developing even more drought resistant crop varieties. Drought resistance might be improved by breeding for a given phenotype to improve overall plant metabolism and resource mobilization (Sawkins et al., 2006). The drought resistance of tropical maize has been considerably increased through classical breeding (Monneveux et al., 2006). A drought resistant maize plant is characterized by reduced plant height, smaller tassels, smaller leaves above the ear, erect leaves, larger stem diameter, stay-green, deeper rooting with less lateral branching and less root biomass, compared to a drought susceptible phenotype (Ribaut et al., 2008).

In the search for the optimal plant phenotype in response to different water regimes, the kinetic of chloroplasts degradation under water-limited conditions, affecting both plant senescence and stay-green, is a critical component (Borrell et al., 2006). This applies also to the tolerance of maize to drought stress at flowering, when stay-green may be associated with better plant water status, with improved pollination, and with higher grain yield through improved kernel set. An association between stay-green at flowering and grain filling is less likely. Thus, stay-green at flowering is a special case, since stay-green usually refers to resistance against drought-induced post-flowering senescence; the term “stay-green” was introduced in sorghum breeding and describes the phenotype of plants that retain their leaves green longer and produce normal grain (Rosenow and Clark, 1981). The stay-green trait is a complex phenomenon, which can be classified in five types, three of which are functional (i.e. are associated with prolonged photosynthesis), while the other two are ‘cosmetic’ rather than functional (Thomas and Howarth, 2000). In practice, the stay-green trait often results from a combination of different types. The expression of stay-green seems to be similar in many crops species, but the genetics and physiology of stay-green are diverse (Thomas and Howarth, 2000).

Senescence, one aspect of stay-green, is a genetically determined process, which can be modulated by external (environmental) factors, for example by drought stress or low nitrogen (N) conditions (Borrás et al., 2003, Masclaux et al., 2001, Muchow and Carberry, 1989, Pearson and Jacobs, 1987). These abiotic stresses alter the source-sink relationship and the (N) status in the plant, both of which are important internal factors regulating senescence (Rajcan and Tollenaar, 1999). Senescence is considered to be a major determinant of grain yield in many crops (He et al., 2005, Thomas, 1992), but the relationship between delayed or reduced senescence and grain yield is not always clear. Moreover, it is not always clear whether the low senescence of a drought tolerant maize genotype is a cause of drought tolerance, a by-product of improved drought tolerance or the result of a more extensive root system (Borrell et al., 2001). The situation is further complicated because senescence is not simply the result of N starvation, but is an active process that requires an adequate supply of carbohydrates (Noodén et al., 1997).

The earliest symptom of senescence is a loss of greenness of leaves, which is due to the loss of chlorophyll, a consequence of the degradation of chloroplasts (He et al., 2005, Smart et al., 1995). The SPAD values recorded with a portable chlorophyll meter provide an indication of the relative amount of total chlorophyll in the leaves, an indicator of foliar senescence. Xu et al. (2000) found highly significant correlations between SPAD values and total chlorophyll (nearly linear relationship) as well as between SPAD values and visual stay-green ratings in grain sorghum. They concluded that arbitrary visual stay-green ratings are a reliable indication of leaf senescence and provide a tool to sorghum breeders to evaluate post-flowering drought tolerance. However, Monneveux et al. (2008) reported that leaf senescence can be used to screen among rather drought-susceptible maize genotypes, but is probably less efficient in material that has already been improved for drought tolerance.

Roots play an important role in the adaptation of maize to drought stress (Lebreton et al., 1995). Unfortunately, it is very difficult to scrutinize the root system of many samples under realistic field conditions. The non-destructive measurement of root capacitance with a portable capacitance meter offers a feasible way of approximating relative differences in the extension of the root system. The capacitance readings correlated strongly and linearly with the fresh mass of maize roots in pot experiments and in the field (van Beem et al., 1998), while Ozier-Lafontaine and Bajazet (2005) found an exponential correlation in the case of progressively immersed root systems of tomato plants. Although the measurement is vulnerable to changes in edaphic factors affecting electrical capacitance, with soil water content being the most important one (Dalton, 1995, van Beem et al., 1998), the degree of genetic control seems to be surprisingly high (Chloupek et al., 2006). Capacitance measurements can be considered as an estimation of root system size and they have been successfully used to map QTLs in barley (Chloupek et al., 2006).

This study identified the genomic regions responsible for the expression of leaf chlorophyll, visual senescence ratings, and root capacitance in a RIL population segregating for the response to water-limited conditions at flowering. To investigate source-sink relationships, the phenotypic results and QTLs of these traits were compared with those of grain yield, yield components and other secondary morphological traits already published (Messmer et al., 2009). The final objective of such efforts is to enhance the understanding of quantitative genetic control of traits related to drought resistance of maize, which is required to sustain breeding progress.