**4. Adaptation of millets to drought**

namely proso millet, little millet, foxtail millet and wild millet [*Setaria glauca* (L.) Beauv.]. Compared to the well-watered plants, a significant yield reduction was obtained in all four millets when the drought treatment was implemented at early developmental stage, that is, before flowering (or heading). However, terminal drought, which occurs from the flowering stage to the harvesting of the crop, contributed to a significant yield loss only in proso and

**Millet type Yield loss (%) Critical stage Reference**

Little millet 62.6\* 80.1\* 80.5\* [51]

Pearl millet 6.6 60.1 Flowering [53] Finger millet 109.8\*f Flowering [54]

**flowering End of flowering**

Tef 69–77 [55]

A study by Winkel et al. [52] in Niger where the annual rainfall is around 200 mm investigated the impact of water deficit at three stages of pearl millet development. The three stages were prior to flowering, at flowering and at the end of flowering. According to the findings of the work, the grain yield of pearl millet was severely reduced when moisture was limited prior to

**droughtc**

27.3\* 15.3NS 30.1\* [51]

heading

Before heading

From four weeks to

flowering [52]

[51]

[51]

little millets while the effect on foxtail and wild millets was negligible.

646 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

Foxtail millet 19.2\* 3.4NS 20.3\*

**Mid-season stressd Terminal stresse**

**Prior to flowering Beginning**

Pearl millet 72 61 Insignificant

**Early stressg**

 Early drought: water stress from 25 days after sowing till flowering. \*Indicates statistically significant difference from the well-watered samples.

 Long-term drought: water stress from 25 days after sowing till harvesting. d Mid-season stress: water stress for 30 days from floral initiation to flowering.

**Table 3.** The magnitude of yield loss due to moisture scarcity in millets.

g Early stress: water stress from two weeks after emergence until symptoms of stress observed.

Terminal drought: water stress from flowering till harvesting.

Terminal stress: water stress at flowering.

Water stress from 28 days after sowing to harvest.

Wild millet (*Setaria gluaca*)

a

b

c

e

f

**Early droughta terminal droughtb Long-term**

Proso millet 30.1\* 34.6\* 64.0\* Before and after

## **4.1. Strategies to drought adaptation or tolerance**

Plants cope with drought using three main strategies, namely, drought escape, drought avoidance and drought tolerance, although a fourth strategy, known as drought recovery, has also been identified [56–60].

**Drought escape:** Drought escape refers to the condition in which plants reach maturity before the drought occurs. Traits associated with drought escape are rapid growth, early flowering, high leaf nitrogen level and high photosynthetic capacity [58]. The study in West Africa indicated that pearl millet matches its phenology to the mean distribution of the rainfall where precipitation is limited and erratic [61]. In this case, the development of the main panicle coincided with an increasing period of rain, thus reducing the risks associated with drought events occurring prior to or at the beginning of flowering.

**Drought avoidance:** Drought avoidance refers to the ability of the plant to maintain a favour‐ able water balance under moisture stress in order to avoid water deficit in the plant tissue. Two types of drought avoidance mechanisms have been identified: (i) those that reduce water loss through transpiration (e.g. low stomata conductance and reduced leaf) and (ii) those that maintain water uptake during drought period (e.g. high root-to-shoot ratio) [56, 58, 62].

**Drought tolerance:** Drought tolerance refers to the ability of the plant to produce some yield by withstanding low water potential [62]. Traits associated with drought tolerance are increased osmoprotectants (or compatible solutes such as betaines and amino acids), and osmotic adjustment (i.e. reducing osmotic potential through accumulation of organic and inorganic substances) [58, 60].

**Drought recovery:** Drought recovery refers to a condition in which plants recover from the adverse effects of drought in order to provide some yield and/or biomass. Desiccation‐tolerant or resurrection plants particularly the wild *Eragrostis nindensis* is the typical example of drought recovery since it stabilizes its cells or membranes at desiccated state [63].

These strategies which are devised by plants to cope with drought are manifested through changes in some phenotypic traits. In a recent review, Kooyers [58] showed for each strategy the path followed by plants in terms of life cycle, altered phenotypes and to the type of drought the plant fits itself. This indicates that the strategies and mechanisms of drought tolerance are interrelated.

#### **4.2. Mechanism of drought tolerance**

Table 4 summarizes various mechanisms of drought tolerance in diverse millet types. These inherent properties of plants which include agronomical, morphological and physiological traits are briefly discussed below.


**Table 4.** Traits associated to diverse drought tolerance mechanisms in millets.

**Agronomy-related traits**: These refer to the traits that are commonly known as yield and yield components. Among these, number of tillers, number and size of panicle, seed and biomass yield, seed weight and harvest index are the major ones. However, conclusions could not be made from the two studies using drought-tolerant pearl millet cultivars since drought did not affectthe shootbiomass inthe first case[64]whileitboostedthe seedyieldinthesecondcase[65].

These strategies which are devised by plants to cope with drought are manifested through changes in some phenotypic traits. In a recent review, Kooyers [58] showed for each strategy the path followed by plants in terms of life cycle, altered phenotypes and to the type of drought the plant fits itself. This indicates that the strategies and mechanisms of drought tolerance are

Table 4 summarizes various mechanisms of drought tolerance in diverse millet types. These inherent properties of plants which include agronomical, morphological and physiological

**Parameter Millet type Response to drought Reference**

Seed number and biomass Pearl millet Unaffected under drought [64] Seed yield Pearl millet High for drought-tolerant genotypes [65] Flowering time Pearl millet Adjust phenology to rainfall pattern [53]

Shoot length Little millet Decreased under drought [40] Root length Little millet Increased under drought [40] Leaf tensile strength Tef Increased in drought-tolerant plants [68]

Chlorophyll content Little millet Decreased under drought [40]

Anti-oxidants Little millet Accumulated under drought [40] ROS scavenging enzymes Little millet, tef Accumulated under drought [40, 71] Free proline Tef, little millet Increased concentration [40, 71] GB (glycine betaine) Little millet Accumulated under drought [40] Superoxide Little millet Accumulated under drought [40] AP (ascorbate peroxidase) Tef, little millet Increased specific activity [40, 71] CAT (catalase) Little millet Accumulated under drought [40] GR (glutathione reductase) Tef Increased concentration [71]

Total free amino acid Little millet Increased concentration [40]

**Table 4.** Traits associated to diverse drought tolerance mechanisms in millets.

extraction after flowering

Tef Increased concentration [71]

[65]

Water extraction Pearl millet Less extraction before flowering; more

interrelated.

**4.2. Mechanism of drought tolerance**

648 Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives

traits are briefly discussed below.

**Agronomy-related traits**

**Morphology-related traits**

**Physiology-related traits**

**Biochemical-related traits**

MDAR (monodehydro-ascorbate

reductase)

**Morphology-related traits**: Morphological or anatomical traits which play important roles in drought tolerance include root- and shoot length and leaf area [66]. However, changes in the morphological and biochemical properties of the flag leaf play a key role in drought tolerance as flag leaves are the primary source of photosynthesis [67]. Mechanical properties of the plant also affect drought tolerance in millets. Balsamo et al. [68] studied the leaf tensile strength or also known as force to tear in three *Eragrostis* species with different levels of tolerance to drought. According to their findings, drought-tolerant *E. curvula* had higher tensile strength values than the moderately drought-tolerant *E. tef*, which in turn had higher values than the drought-susceptible *E. capensis*, indicating a positive correlation between drought tolerance and leaf tensile strength [68]. Structural investigations of leaves from the three species revealed the presence of extensive lignification of bundle sheath extensions in *E. tef* and *E. curvula* unlike in *E. capensis*. A study in maize indicated that lignification of the midrib parenchyma and epidermis was directly correlated with increased tensile strength [69].

**Physiology-related traits**: Among the several physiological traits that are differentially regulated during moisture deficit, osmotic adjustment is a major mechanism that increases drought avoidance to enable the plant produce some yield. Osmotic adjustment, which refers to the lowering of the osmotic potential in the cytoplasm due to the accumulation of compatible solutes such as proline, glycine betaine and organic acids, contributes to turgor maintenance of shoots and roots [40]. In little millet, drought stress increased the amount of proline and glycine betaine in both the root and leaf [40]. According to the authors, the accumulation of free amino acids in this millet during drought might be related to the disruption in protein synthesis, induced proteolysis or its partial hydrolysis [40].Water-use efficiency of the plant is also important as moisture is mostly limited in the areas where millets are extensively cultivated. The experiment using drought-sensitive and drought-tolerant pearl millet geno‐ types showed that under moisture deficit conditions, the total amount of water extracted by both genotypes was comparable [65]. However, compared to susceptible genotypes, tolerant genotypes extracted less water prior to flowering and more water after flowering, enabling these genotypes to support the tillers and maintain the stay-green phenotype.

**Biochemical-related traits**: Reactive oxygen species (ROS) are chemically reactive molecules that are useful in cell signalling at low concentrations but are damaging to cells when present at high concentrations. The main causes for the high production of ROS are environmental stresses such as drought and salinity [70]. In order to reduce the damaging effects of ROS, plants produce antioxidants, which include glutathione, ascorbate and carotenoids and ROSscavenging enzymes which include superoxide dismutase (SOD), peroxidase (POD), catalase (CAT) and ascorbate peroxidase (AP or APX) [40]. In little millet, the activity of SOD, POD and CAT were elevated under drought conditions to enable the plant cope with unfavourable ROS accumulation [40]. Similarly, the activity of AP and monodehydro-ascorbate reductase (MDAR) increased in tef plants treated with drought compared to control plants receiving normal watering [71].

### **4.3. Genes involved in drought tolerance**

The sequence of the genome and transcriptome of plants provides information important to the understanding of the types of genes involved in the regulation of drought tolerance, particularly in plants with increased resistant to moisture scarcity. So far, the genome of foxtail millet [72, 73] and tef [3] has been sequenced.

Transcriptome sequencing of millets after exposure to moisture-deficit condition provides information on genes differentially regulated under exposure to abiotic stresses particularly to drought. A transcriptome-wide study of finger millet plants exposed to drought obtained 2824 genes that were differentially expressed under these conditions [74].

Genes known to be involved in drought response and/or tolerance of selected millets are presented in Table 5. Wang et al. [75] indicated that the overexpression of SiLEA14, a type of LEA gene from foxtail millet, increased the tolerance of *Arabidopsis* plants to salt and osmotic stress. Parvathi et al. [76] reported the induction of several genes when finger millet was exposed to drought. The up-regulated genes include metallothionein, farnesylated protein ATFP6, Farnesyl pyrophosphate synthase and protein phosphatase 2A.


**Table 5.** Differentially regulated drought-related genes in millets.

Traits associated with drought tolerance were investigated using a genome scan and associa‐ tion mapping methods [77, 78]. A single gene known as β-carbonic anhydrase (*Pg*CA) was consistently up-regulated in pearl millet exposed to multiple abiotic stresses including drought, salinity and heat [79]. Hence, this particular gene is useful in adapting the plant to diverse abiotic stresses. Other genes known to be involved in drought response or tolerance in millets were EcDehydrin 7 [80], mt1D [81] and Ec-apx1 [82] from finger millet, and SiARDP [83] from wild foxtail millet.

Although not yet reported for millets, the suppression of two genes, namely, SAL1 and ERA1, increased the drought tolerance of the model plant *Arabidopsisthaliana* [84, 85]. The *era1* mutants develop tolerance to drought through a mechanism involving closing of the stomata [85].
