Effect of Drought on Storage Root Development and Gene Expression Profile of Sweetpotato under Greenhouse and Field Conditions

Authors:
Julio Solis School of Plant, Environmental, and Soil Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA 70803

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Arthur Villordon Sweet Potato Research Station, Louisiana State University Agricultural Center, 130 Sweet Potato Road, Chase, LA 71324

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Niranjan Baisakh School of Plant, Environmental, and Soil Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA 70803

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Don LaBonte School of Plant, Environmental, and Soil Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA 70803

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Nurit Firon Institute of Plant Sciences, The Volcani Center, ARO, P.O. Box 6, Bet Dagan, 50250, Israel

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Abstract

Greenhouse and field culture systems were used to study the effect of drought conditions on the storage root (SR) formation in ‘Beauregard’ sweetpotato (Ipomoea batatas). In the greenhouse culture system, drought was simulated by withholding water for 5 and 10 days after transplanting (DAT) cuttings in dry sand. Control plants received water at planting and every 3 days thereafter. In the field studies, natural drought conditions and selective irrigation were used to impose water deprivation during the critical SR formation period. Greenhouse drought for 5 and 10 DAT reduced the number of SRs by 42% and 66%, respectively, compared with the controls. Field drought resulted in a 49% reduction in U.S. #1 SR yield compared with the irrigated condition. Quantitative real-time polymerase chain reaction (PCR) analysis showed differential expression of a set of sweetpotato transcription factors and protein kinases among greenhouse-grown plants subjected to well-watered conditions and water deficit during 5 DAT. A significant enhancement of expression was observed for known drought stress-associated genes such as an abscisic acid-responsive elements-binding factor, dehydration-responsive element-binding factor, and homeo-domain-zip proteins. Members of calcium-binding proteins showed differential expression under drought stress. For the first time it is reported that knotted1-like homeobox and BEL1-like genes showed altered expression in response to drought stress under a greenhouse condition. In summary, the results suggest that water deprivation during the SR formation period influences root development and expression patterns of stress-responsive genes and those previously found associated with SR formation in sweetpotato.

Drought stress represents a global constraint for sweetpotato production because most of the sweetpotato production occurs in semiarid regions (Saraswati, 2007). Considering the complexity of the physiological and genetic mechanisms associated with stress tolerance, a genomics-based understanding of the stress response of sweetpotato will help us develop strategies to sustain its productivity in stressful environments (Boyer, 1982). Candidate drought-responsive genes, identified through genomics research, will have great use in widening the natural allelic variation and its possible use for crop improvement (Rus et al., 2006). However, sweetpotato has lagged with respect to studies leading to the identification of its drought-responsive genes. One study reported 12 genes in response to drought stress in white fibrous roots (Kim et al., 2009), and most of these genes are similar to ones that are known to be associated with dehydration response in many other species. A dehydration responsive element-binding protein gene, a member of the AP2 (Apetala2)/EREBP (ethylene-responsive element binding protein) family, has been characterized in drought-stressed roots and stems of sweetpotato (Kim et al., 2008). Evidence of the genetic basis of sweetpotato tolerance to drought comes from studies carried out in vitro along with field and greenhouse experiments (Ekanayake and Dodds, 1993; Ricardo, 2011). Genes associated with antioxidant activity were up-regulated in leaves under drought and salt stress (Kim et al., 2013). Similarly, transcripts of late embryogenesis abundant proteins, known to be associated with abiotic stress responses, were increased with lignification in sweetpotato tissue cultures (Park et al., 2011). These studies collectively demonstrate that abiotic cues result in transcriptional changes in sweetpotato. However, gene expression under stress has not been studied in early stages of storage root development, before thickening of roots.

Sweetpotato SRs develop from adventitious roots emerging from root primordia located on stem nodes. Unknown intrinsic and extrinsic factors trigger thickening of these adventitious roots, the process known as SR initiation. SR initiation has been defined as the formation of a cambium ring and appearance of anomalous cambia around discrete xylem and protoxylem elements within 20 d of the emergence of an adventitious root (Togari, 1950). Greenhouse and field culture systems in ‘Beauregard’ validated that SR initiation consistently occurred during the first 20 d after transplanting (Villordon et al., 2009a, 2009b). Preformed primordia that produce adventitious roots with pentarch, hexarch, or septarch steles have the potential to develop into SRs (Villordon et al., 2009b). However, damage to the root primordia, unfavorable edaphoclimatic conditions, and age of nodes influence the total SR in a cultivar.

Although previous molecular studies during the past decade have reported several candidate genes to be up-regulated or expressed preferentially in SRs, no single gene has been shown to be solely responsible for conversion of the adventitious roots into storage organs (Kim et al., 2002, 2005; Ku et al., 2008; Noh et al., 2010; Tanaka et al., 2008; You et al., 2003). Most of these genes have either regulatory roles as transcription factors or are involved in carbohydrate and protein metabolism during the development and thickening of the SRs. Firon et al. (2013) have recently demonstrated down-regulation in the expression of key genes of the phenylpropanoid biosynthesis pathway on the change in root fate from fibrous root to a storage organ. In addition, precise control at the level of gene expression of regulators of meristematic tissue identity and maintenance, up-regulation of cell-division regulators, and down-regulation of specific GRAS [GAI (gibberellin acid-insensitive), RGA (repressor of GA1), SCR (scarecrow)] family members in the SR-initiation process were indicated.

The present study was undertaken to examine the effect of drought stress on the SR formation under greenhouse and field conditions and to characterize the expression of a selected set of genes in root tissues of drought-stressed vs. non-stressed plants. The genes included in this study were selected based on their 1) role in gene regulation and calcium signaling during developmental and physiological processes; 2) enrichment in root libraries (GenBank; Firon et al., 2013; Schafleitner et al., 2010); 3) role in drought stress responses and hormone signaling; and 4) functional homology to genes known to be involved in storage organ development in other crops such as potato [Solanum tuberosum (Reddy et al., 2002)] and cassava [Manihot esculenta (de Souza et al., 2004)].

Materials and Methods

Plant material.

Sweetpotato plant cuttings (≈20 cm long) were obtained from generation 0 (derived from in vitro cultures) virus-tested, greenhouse-grown ‘Beauregard’ for greenhouse studies and virus-tested generation 1 seed roots in plant beds for field studies.

Drought studies under greenhouse conditions.

Unrooted cuttings (n = 9 for each of the three treatments) were prepared and transplanted the same day in dry sand in cylindrical tubes (50 × 9.82 cm) under greenhouse conditions. Plants were grown inside the greenhouse under a day/night temperature regime of 27/21 °C for Trial 1 (30 Jan. 2011 to 10 Mar. 2011) and 28/25 °C for Trial 2 (9 May 2011 to 21 June 2011), respectively, at 50 to 70 μmol·m−2·s−1; no artificial lighting was provided. Our earlier pilot experiments indicated that the cuttings could survive at least 10 DAT into dry sand under controlled conditions.

Drought stress was imposed by withholding water for 5 and 10 DAT and control plants received water the same day of transplanting (0 DAT). Subsequently, stressed plants received water every 3 d, whereas the control plants received water every 3 d throughout the experiment. Each treatment included nine plants. Cuttings were watered (400 mL) every 3 d after the initial 5- and 10-d treatment period. Water-soluble 20N–8.7P–16.6K solution (Peters Professional Soluble Plant Food; Scotts-Sierra, Marysville, OH) was applied (0.374 g/200 mL) at 12 and 22 DAT. Four weeks after transplanting, the plants were evaluated for the number of SRs (width greater than 1.5 mm) and the width and weight of the SRs. Thin pigmented roots (width less than 1.5 mm) were included in the total count of SRs (SRCount1) because we considered them as putative-forming/developing SRs. A second count of SRs (SRCount2) excluded these pigmented SRs. Maximum diameters of SRs were measured with a caliper. The experiments were repeated twice.

A second study was carried out in the greenhouse to evaluate expression of a set of selected genes (Table 1) in total roots from initially drought-stressed (no water for 5 DAT) and well-watered (control) plants. The initial water stress at planting may resemble unfavorable drought conditions met by farmers, where cuttings are left in soil without watering until rainfall arrives. Fertilizer was applied at 12 DAT. Roots from these plants were sampled at 14 DAT in triplicate by pooling roots from three plants and then the roots were frozen in liquid nitrogen. Root tissues were stored at –80 °C; the experiment was repeated twice.

Table 1.

Annotation and primer sequences of the genes used for expression analysis in sweetpotato roots.

Table 1.

Drought studies under field conditions.

Field experiments were conducted in the Summer 2010 and 2011 in well-drained research fields at Chase, LA (lat. 32°6′ N, long. 91°42′ W). The soil taxonomic class was fine-silty, mixed, active, thermic Typic Glossaqualfs. There were three planting dates in 2010 (12 May, 27 May, and 3 June) and two planting dates in 2011 (19 May and 1 June). In each year, natural rainfall deficits during May and June created conditions where soil moisture in the root zone was near the wilting point for the soil type used in the studies. The rainfall pattern during the time of experiments in 2010 and 2011 is shown in Figure 1. Rickard and Fitzgerald (1969) defined agricultural drought as existing when the soil moisture in the root zone is at or below wilting point. During June to Aug. 2011, portions of northeastern Louisiana, including the location of the field experiments, had record low values for the Palmer hydrological drought index in the 117-year record (Blunden and Arndt, 2012). These growing conditions were used to compare SR yield from plots with drought-stressed (non-irrigated) vs. plots that were irrigated to maintain soil moisture at 50% of field capacity (FC) during the SR initiation phase, which can occur as early as 13 DAT in ‘Beauregard’ grown in field plots (Villordon et al., 2009b). Field preparation activities, including fertilizer rates, herbicide, and insecticide applications, were similar in each year as previously described (Villordon et al., 2009b, 2011). Supplemental overhead irrigation was supplied with a traveling irrigation sprinkler if a rainfall event did not occur in irrigated plots.

Fig. 1.
Fig. 1.

Rainfall data of Chase, LA, during the experiments of 2010 and 2011 to study the effect of drought stress on storage root yield of sweetpotato (National Oceanic and Atmospheric Administration, 2014).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 139, 3; 10.21273/JASHS.139.3.317

In each planting date, two plots were designated as irrigated vs. non-irrigated plots. Plot size was 12 rows × 30 m on 1-m centers. The plots were separated by a buffer zone equivalent to 12 rows. Supplemental irrigation was based on soil moisture sensor data and irrigation was applied when soil moisture at the 15-cm depth approached 25% of FC. A 16% volumetric water content (VWC) represented 50% of FC in this study. This soil moisture range has previously been calibrated (Constantin et al., 1974) and validated (Villordon et al., 2010) as optimum for ‘Beauregard’ grown in north Louisiana. Soil moisture monitoring at two depths (5 and 15 cm) was performed by vertically installed soil moisture sensors (Model 5TE; Decagon Devices, Pullman, WA) linked to automated data loggers (EM50; Decagon Devices). All supplemental irrigation was delivered through a traveling irrigation sprinkler or furrow irrigation (after 35 DAT). For non-irrigated plots, soil moisture was consistently below or at levels defined as the wilting point during the SR formation period. In 2010, soil moisture at the 15-cm depth stayed below 10% VWC during the first 30 d of growth in non-irrigated plots. This range has been previously defined as the witling point for this soil type (Ley et al., 1994). In 2011, soil moisture at the 15-cm depth ranged from 9% to 11% VWC during the first 30 d of growth in non-irrigated plots. All plots subsequently received natural rainfall events, which precluded supplemental irrigation. At harvest, a two-row section (6 m in length) located in the center of each plot was designated as the record rows and used for SR yield measurements. Harvest was at 110 DAT (2010) to 130 DAT (2011) and SRs were graded according to U.S. Department of Agriculture standards (USDA, 2005): U.S. #1 (5.1 to 8.9 cm diameter and 7.6 to 22.9 cm length), Canner (2.5 to 5.1 cm diameter and 5.1 to 17.8 cm length), and Jumbo (larger than both groups). Total marketable yield was defined as the sum of U.S. #1, Canner, and Jumbo. The number of SRs classified as U.S. #1 grade, the premium yield grade, was also counted.

Gene expression profiling by quantitative reverse transcription PCR (qRT-PCR).

RNA was extracted from 2-week-old root tissues using the RNeasy plant minikit (Qiagen, Valencia, CA) following the vendor’s protocol. An on-column DNase I treatment was done to eliminate any contaminating DNA. RNA quality and quantity were determined using a spectrophotometer (NanoDrop ND-1000; Thermo Scientific, Wilmington, DE). cDNA synthesis and quantitative reverse transcription (qRT)–PCR were performed as described earlier (Effendy et al., 2013). Briefly, 2 μg of total RNA was reverse transcribed using an iScript cDNA synthesis kit (Bio-Rad, Hercules, CA). The first strand cDNA was diluted three times with water, and 2 μL was used for the PCR using the iQSYBR green supermix (Bio-Rad). A melting curve analysis was performed to ensure correct gene amplification product. The sweetpotato elongation factor 1-alpha [IbEF1a (Effendy et al., 2013)] (Table 1) was used as the reference gene for normalization of gene expression. Each qRT-PCR reaction was run in triplicate and each gene was tested twice using cDNA made from two independent RNA sample sets from total roots (drought and control). Fold change expression of the genes under drought and control conditions was calculated using the 2-ddct method (Effendy et al., 2013). Primers specific to the 19 genes, including 2 KNOX genes [Ibkn2, Ibkn3 (Tanaka et al., 2008)], used for expression analysis under drought vs. control samples are described in Table 1. Transcription factors such as BELL (IbBEL1, IbBEL2, IbBEL3) and Knox (IbKn2, IbKn3a, IbKn3b) genes were selected because of their role in tuber development in potato (Chen et al., 2003) and sweetpotato and abundance of Knox genes in sweetpotato (Firon et al., 2013; Tanaka et al., 2008). Homeobox domain-containing proteins (IbHB1, IbHB2) and general regulatory factor (IbGRF) were included in the study because of their preponderance in initiating SRs (Firon et al., 2013; Solis, 2012). Cytokinin response genes (IbCRF1, IbCRF2) were selected because of the role of cytokinin in inducing SR formation (Eguchi and Yoshida, 2008). Abscisic acid responsive element binding protein (IbAREB) and dehydration responsive element binding protein (IbDREB1) genes were selected considering their role in plant responses to abiotic stresses (Choi et al., 2000, 2005). Genes associated with calcium signaling (IbCBP1, IbCBP2, IbCDPK3) and signal transduction (IbTAP) were chosen because of their abundance in the developing storage organ of sweetpotato (Solis, 2012) and potato (Pais et al., 2010; Poovaiah et al., 1996; Raices et al., 2003; Reddy et al., 2002). The accession numbers of the expressed sequence tags used for designing primers for this study are provided in Table 1.

Experimental design and statistical analyses.

The greenhouse experiments were conducted in a completely randomized design, whereas the field experiments were conducted as a randomized complete block design using planting dates as replicates. Data were analyzed using the Proc GLM module in SAS (SAS Institute, Cary, NC).

Results

Drought stress studies under greenhouse conditions.

Drought stress treatment in two separate greenhouse trials showed a negative effect on the growth of sweetpotato SRs (Table 2). A reduction in the number, size, and weight of SRs was observed in the drought-stressed plants in comparison with the control plants. The number of SRs (SRCount1), which included all thickened and pigmented (putative) SRs, decreased by 43% in Trial 1 and by 30% in Trial 2 under moderate 5 DAT drought stress (Table 2). Using more conservative counts [SRCount2 (excluding pigmented putative forming SRs)], the reductions were 42% and 29% in Trials 1 and 2, respectively, between 5 DAT drought stress vs. control plants. The reduction in SRCount1 at 10 DAT drought stress was greater compared with that at 5 DAT drought stress with a reduction of 59% and 67% in both Trial 2 and Trial 1, respectively. The SRCount2 at 10 DAT drought stress showed a reduction of 71% in Trial 1 and 62% in Trial 2.

Table 2.

Effect of drought stress under greenhouse conditions on sweetpotato storage root growth.z

Table 2.

All plants reached similar foliar growth at the time of harvest and no death occurred as a result of drought stress under greenhouse conditions. Plants under drought stress showed moderate to severe stress effects in terms of reduction of weight and the maximum diameter of the SRs compared with the control. For example, the weight of the SRs was 50% and 73% less in plants experiencing 5 and 10 DAT drought stress, respectively, in comparison with the control in Trial 1 (Table 2). Reduction in SR weight followed a similar trend in Trial 2 (Table 2). Maximum diameter of the SRs was 13% and 51% less in plants experiencing drought stress of 5 and 10 DAT, respectively, in comparison with the control in Trial 1. Reductions were more pronounced in Trial 2.

Drought stress studies under field conditions.

The results of field experiments of combined data from 2010 and 2011 seasons showed that the yield of sweetpotato plants experiencing drought stress under field conditions was reduced significantly (Table 3). The yield reduction was most pronounced for the important U.S. #1 grade; non-irrigated plots showed a 49% yield reduction compared with the irrigated plots. The total marketable root yield showed similar trends with a reduction of 43% in the non-irrigated plots compared with the control. The jumbo and medium grades were not significantly different and consistent with high replication variability typically encountered in sweetpotato yield studies.

Table 3.

Combined storage root yield of sweetpotato in response to irrigation treatments under field conditions after 110 d (in 2010) and 130 d (in 2011) of growth, Chase, LA.

Table 3.

Gene expression under greenhouse drought stress.

Ten of 19 genes tested were found up-regulated in drought-stressed roots with fold change expression of at least 1.4 relative to control (IbAREB; IbBEL1, 2, 3; IbCBP2; IbCRF1; IbHB1, 2; IbKn2, 3a), and only two genes (IbCBP1 and IbCDPK3) were down-regulated (Fig. 2). Expression levels for IbBEL2, Ibkn2, and IbCRF2 genes correspond to a single set of triplicate sample treatments, and for the rest of the genes, the expression levels are as described in “Materials and Methods” (two independent sets of triplicate samples). Of the up-regulated genes, nine were transcription factors and the other (IbCBP2) coded for a calcium-binding protein.

Fig. 2.
Fig. 2.

Expression profile of 14 genes in sweetpotato roots from 2-week-old plants under greenhouse drought stress (5 d after transplanting) vs. control by quantitative real-time polymerase chain reaction. Error bars represent sem of two independent experiments averaged over three replications each except IbBEL2, Ibkn2, and IbCRF2, where the se was calculated over the mean of three replicates in a single experiment. Fold change in expression of the genes was determined by normalizing the values against that of the reference gene IbEF1a and calculated relative to the control that was set to 1.0.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 139, 3; 10.21273/JASHS.139.3.317

Three genes, IbHB2 (encoding a homeobox protein), IbCRF1 (encoding a protein similar to the Arabidopsis thaliana cytokinin response factor 1), and IbAREB (encoding an abscisic acid-responsive elements-binding factor), showed very high accumulation of their transcripts under drought stress imposed 5 DAT in comparison with the control. The greatest increase in abundance of transcript under drought stress was observed for IbHB2.

BELL (IbBEL1, IbBEL2, and IbBEL3) and KNOX (Ibkn3a) transcription factors were up-regulated 1.4- to 2.2-fold in roots of plants that were under drought stress. Two genes, IbDREB1 and IbGRF, did not show significant differences in their expression between roots of drought-stressed and control plants, whereas expression changes of IbSnRK and IbTAP were inconsistent (data not shown).

Of the down-regulated genes, only IbCBP1, encoding a calcium-binding protein, showed the greatest reduction of expression up to 80% (fold change 0.22) in roots under greenhouse drought stress compared with the control, and a slight decrease (fold change 0.76) of transcript abundance was observed for IbCDPK3, a gene putatively encoding a calcium-dependent protein kinase (Fig. 2).

Discussion

Drought and storage root.

Drought stress under greenhouse conditions significantly reduced the number, size, and weight of sweetpotato SRs compared with the control plants (Table 2). The 5 DAT treatments showed a 30% to 42% reduction in SR number across the two studies. SR numbers were reduced further (up to 66%) by extending the drought period to 10 DAT. Results at 5 and 10 DAT were consistent over two sets of experiments and demonstrated the effect soil moisture could exert on SR formation. Preliminary experiments carried out in growth chambers in 2008 and 2009 under controlled conditions of humidity, daylight, and temperature had a similar outcome (Solis, 2012).

The 2010 and 2011 growing seasons in Louisiana were characterized by prolonged periods without rainfall, especially during the critical period of SR initiation in field-grown ‘Beauregard’ (Villordon et al., 2009b). This growing environment allowed for the comparison of irrigated vs. non-irrigated treatments on SR initiation and subsequent SR bulking without the confounding effects of natural rainfall events.

In each year, there was marginal soil moisture (less than 25% to 50% of FC) during the transplanting phase in the non-irrigated plots. This allowed for some SR initiation; however, the lack of additional soil moisture up to 30 DAT impacted further development, resulting in low SR count and delayed SR development. At harvest (110 to 130 DAT), irrigated plots showed over a 100% increase in U.S. #1 yield relative to non-irrigated (up to 30 DAT) plots (Table 3). Adequate soil moisture after 30 d did not overcome the effects of the initial drought. These data corroborated earlier findings of Togari (1950) that provided evidence that environmental and management variables during the first 20 DAT exert considerable influence on SR formation, dictating the future yield of the crop.

The reduction of yield and quality of roots observed in the non-irrigated field and the reduced number, diameter, and weight of SRs under greenhouse drought conditions support our hypothesis that lack of soil moisture irreparably alters root development toward non-storage-forming roots.

Gene expression.

Several key genes were shown to be involved in sweetpotato SR development by comparing storage and non-storage-forming roots (Firon et al., 2013; Kim et al., 2002, 2005; Ku et al., 2008; Noh et al., 2010; Tanaka et al., 2008; You et al., 2003). Kim et al. (2009) focused primarily on the identification and study of genes from fibrous roots under drought stress at the late growth stage. The present study focused on gene expression profile of 2-week-old total root pools from non-stressed and drought-stressed plants (5 DAT) at an early stage of growth. The genes included in this study were selected based on comparative analysis of the available sweetpotato root transcriptome (Firon et al., 2013), expressed sequence tag sequences deposited at GenBank and PlantGDB, and sequences from leaf and stem libraries of drought-stressed sweetpotato plants (Schafleitner et al., 2010).

Homeobox leucine zippers, AP2/EREBP, and abscisic acid responsive-like genes.

Among the genes that had the highest up-regulation in sweetpotato roots under drought stress were IbHB2, IbCRF1, and IbAREB (Fig. 2). The sweetpotato gene IbHB2 is an ortholog of ATHB7 (At2g46680) and a member of the homeobox leucine zipper transcription factors (HD-Zip). Transcripts of ATHB7accumulated in response to water stress in A. thaliana (Olsson et al., 2004; Soderman et al., 1996). HD-Zip genes are implicated in both developmental changes and stress responses in A. thaliana (Hjellström, 2002; Lee and Chun, 1998; Soderman et al., 1999) and cassava (Lokko et al., 2007) and dehydration tolerance in the root and leaves of resurrection plant [Craterostigma plantagineum (Deng et al., 2002)]. Furthermore, gradual reduction of expression of the cotton (Gossypium hirsutum) HD-Zip gene (GhHB1) with development of roots and its induction in response to abscisic acid and salt (Ni et al., 2008) indicated that HD-Zip genes play important roles in both morphogenic processes as well as stress responses of plants.

The sweetpotato gene IbCRF1 that showed the second highest increase in expression (fold change of 6) under drought stress is similar to AP2/EREBP genes (Riechmann and Meyerowitz, 1998) and cytokinin response genes (Rashotte and Goertzen, 2010). Expression of many members of the AP2/EREBP gene family is altered in response to abiotic (Chen et al., 2007; Kim et al., 2008; Kizis et al., 2001; Xiong et al., 2002) and biotic stresses (Lin et al., 2007). Although CRF-like genes have not been studied previously in sweetpotato, cytokinins were shown to induce SR organs in sweetpotato (Eguchi and Yoshida, 2008). Therefore, it is presumed that IbCRF1, being a cytokinin responsive gene, could play an important role in SR development under water stress.

Homeobox Bell and KNOX I genes.

KNOX (knotted1-like homeobox) genes have been previously found to be associated with the formation of SRs (Tanaka et al., 2008). In the present study, three BELL (BEL1-Like) genes IbBEL1, IbBEL2, and IbBEL3, and KNOX genes Ibkn1, Ibkn2, and Ibkn3 were up-regulated ≈1.4 to two times in 2-week-old sweetpotato roots in response to drought stress (Fig. 2). In sweetpotato, two variants of Ibkn3 (Ibkn3a and Ibkn3b) were identified (Solis, 2012). Ibkn3a showed ≈2-fold higher expression under drought over a control, whereas Ibkn3b was slightly down-regulated under drought stress (fold change of 0.88). BELL and KNOX proteins are known to interact during potato tuberization (Chen et al., 2003), IbCRF1 and IbCRF2, under drought stress. Further functional characterization of the cytokinin signaling by KNOX and BELL genes is required in sweetpotato to understand the mechanism of their role in abiotic stress response and SR development.

Calcium signaling genes.

In the present study, the IbCBP2 gene, an ortholog of A. thaliana iqd9 (At2g33990) encoding calmodulin binding protein, was up-regulated (fold change of 2.12), whereas two other genes encoding calcium-binding proteins, IbCBP1 and IbCDPK3, were down-regulated under drought stress. CBP-like genes were shown to be involved in potato tuberization (Poovaiah et al., 1996; Reddy et al., 2002). Similarly calcium-binding proteins such as CDPKs and calcineurin-B-like genes were shown to be induced by drought and salt stresses (Jimenez et al., 2008). Therefore, it remains to be seen if strict regulation of CBP-like genes are required to trigger SR formation in sweetpotato by modulating other downstream stress-related genes under drought stress (Albrecht et al., 2003; Cheong et al., 2003).

Other regulatory genes.

Genes such as IbGRF and IbDREB1 did not show significant differences between roots of drought-stressed and control plants, but these genes (IbDREB1, IbGRF, IbSnRK, and IbTAP) were shown be abundant in SR libraries compared with that from lignified roots based on their digital expression profile in sweetpotato root (Solis, 2012). Inconsistent expression observed for IbSnRK and IbTAP between replicates in the present study was attributed to the difference in greenhouse temperatures during growth stages and at root sampling.

Conclusions

The present study showed drought stress significantly affects SR number and development in sweetpotato. The expression of genes (IbHB2, IbCRF1, and IbAREB), not previously documented in sweetpotato, were significantly altered in response to drought stress as observed in other species. This work furthermore demonstrated, for the first time, that genes such as IbBEL1, IbBEL2, IbBEL3, IbHB2, and Ibkn3a are stress-responsive genes and are up-regulated in roots under greenhouse drought stress conditions. The overall results indicated that genes known to be associated with the onset of bulking are sensitive to drought stress and the consequence is a diminished number of sweetpotato SRs under stress. Altered expression of transcripts of signaling genes (IbCBP1, IbCBP2, and IbCDPK3) could be related to the reduced number of SRs. Detailed studies are required to precisely determine the role of up-regulated genes in SR under drought stress, which could potentially be used as biomarkers to identify the effect of water stress on SR development.

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  • Eguchi, T. & Yoshida, S. 2008 Effects of application of sucrose and cytokinin to roots on the formation of tuberous roots in sweetpotato [Ipomoea batatas (L.) Lam.] Plant Root 2 7 13

    • Search Google Scholar
    • Export Citation
  • Ekanayake, I.J. & Dodds, J.H. 1993 In vitro testing for the effects of salt stress on growth and survival of sweetpotato Sci. Hort. 55 239 248

  • Firon, N., LaBonte, D., Villordon, A., Kfir, Y., Solis, J., Lapis, E., Perlman, T.S., Doron-Faigenboim, A., Hetzroni, A., Althan, L. & Nadir, L.A. 2013 Transcriptional profiling of sweetpotato (Ipomoea batatas) roots indicates down-regulation of lignin biosynthesis and up-regulation of starch biosynthesis at an early stage of storage root formation BMC Genomics 14 460

    • Search Google Scholar
    • Export Citation
  • Hjellström, M. 2002 Drought stress signal transduction by the HD-Zip transcription factors ATHB6 and ATHB7. Acta Universitatis Upsaliensis. Comprehensive Summaries Uppsala diss., Faculty Sci. Technol. 690:18

  • Jimenez, J.A., Alonso-Ramirez, A. & Nicolas, C. 2008 Two cDNA clones (FsDhn1 and FsClo1) up-regulated by ABA are involved in drought responses in Fasus sylvatica L. seeds J. Plant Physiol. 165 1798 1807

    • Search Google Scholar
    • Export Citation
  • Kim, S.H., Hamada, T., Otani, M. & Shimada, T. 2005 Isolation and characterization of MADS box genes possibly related to root development in sweetpotato (Ipomoea batatas L. Lam.) J. Plant Biol. 48 387 393

    • Search Google Scholar
    • Export Citation
  • Kim, S.H., Mizuno, K. & Fujimura, T. 2002 Isolation of MADS-box genes from sweet potato [Ipomoea batatas (L.) Lam.] expressed specifically in vegetative tissues Plant Cell Physiol. 43 314 322

    • Search Google Scholar
    • Export Citation
  • Kim, S.H., Song, W.K., Kim, Y.H., Kwon, S.Y., Lee, H.S., Lee, I.C. & Kwak, S.S. 2009 Characterization of full-length enriched expressed sequence tags of dehydration-treated white fibrous roots of sweetpotato BMB Rpt. 42 271 276

    • Search Google Scholar
    • Export Citation
  • Kim, Y.H., Jeong, J.C., Lee, H.S. & Kwak, S.S. 2013 Comparative characterization of sweetpotato antioxidant genes from expressed sequence tags of dehydration-treated fibrous roots under different abiotic stress conditions Mol. Biol. Rpt. 40 2887 2896

    • Search Google Scholar
    • Export Citation
  • Kim, Y.H., Yang, K.S., Ryu, S.H., Kim, K.Y., Song, W.K., Kwon, S.Y., Lee, H.S., Bang, J.W. & Kwak, S.S. 2008 Molecular characterization of a cDNA encoding DRE-binding transcription factor from dehydration-treated fibrous roots of sweetpotato Plant Physiol. Biochem. 46 196 204

    • Search Google Scholar
    • Export Citation
  • Kizis, D., Lumbreras, V. & Pages, M. 2001 Role of AP2/EREBP transcription factors in gene regulation during abiotic stress FEBS Lett. 498 187 189

  • Ku, A.T., Huang, Y.S., Wang, Y.S., Ma, D. & Yeh, K.W. 2008 IbMADS1 (Ipomoea batatas MADS-box 1 gene) is involved in tuberous root initiation in sweet potato (Ipomoea batatas) Ann. Bot. (Lond.) 102 57 67

    • Search Google Scholar
    • Export Citation
  • Lee, Y.H. & Chun, J.Y. 1998 A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment Plant Mol. Biol. 37 377 384

    • Search Google Scholar
    • Export Citation
  • Ley, T.W., Stevens, R.G., Topielec, R.R. & Neibling, W.H. 1994 Soil water monitoring and measurement. Washington State Univ., Pacific Northwest Ext. Publ. 475

  • Lin, R., Zhao, W., Meng, X. & Peng, Y.L. 2007 Molecular cloning and characterization of a rice gene encoding AP2/EREBP-type transcription factor and its expression in response to infection with blast fungus and abiotic stresses Physiol. Mol. Plant Pathol. 70 60 68

    • Search Google Scholar
    • Export Citation
  • Lokko, Y., Anderson, J.V., Rudd, S., Raji, A., Horvath, D., Mikel, M.A., Kim, R., Liu, L., Hernandez, A., Dixon, A.G.O. & Ingelbrecht, I.L. 2007 Characterization of an 18,166 EST dataset for cassava (Manihot esculenta Crantz) enriched for drought-responsive genes Plant Cell Rpt. 26 1605 1618

    • Search Google Scholar
    • Export Citation
  • National Oceanic and Atmospheric Administration 2014 Monthly climatological summary 2010, 2011. 1 Jan. 2014. <http://www.ncdc.noaa.gov/cdo-web/datasets/GHCNDMS/stations/GHCND:USC00169806/detail>

  • Ni, Y.X., Wang, X.L., Li, D.D., Wu, Y.J., Xu, W.L. & Li, X.B. 2008 Novel cotton homeobox gene and its expression profiling in root development and in response to stresses and phytohormones Acta Biochim. Biophys. Sin. (Shanghai) 40 78 84

    • Search Google Scholar
    • Export Citation
  • Noh, S.A., Lee, H.S., Huh, E.J., Huh, G.H., Paek, K.H., Shin, J.S. & Bae, J.M. 2010 SRD1 is involved in the auxin-mediated initial thickening growth of storage root by enhancing proliferation of metaxylem and cambium cells in sweetpotato (Ipomoea batatas) J. Expt. Bot. 61 1337 1349

    • Search Google Scholar
    • Export Citation
  • Olsson, A.S.B., Engstrom, P. & Soderman, E. 2004 The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis Plant Mol. Biol. 55 663 677

    • Search Google Scholar
    • Export Citation
  • Pais, S.M., Garcia, M.N., Tellez-Inon, M.T. & Capiati, D.A. 2010 Protein phosphatases type 2A mediate tuberization signaling in Solanum tuberosum L. leaves Planta 232 37 49

    • Search Google Scholar
    • Export Citation
  • Park, S.C., Kim, Y.H., Jeong, J.C., Kim, C.Y., Lee, H.S., Bang, J.W. & Kwak, S.S. 2011 Sweetpotato late embryogenesis abundant 14 (IbLEA14) gene influences lignification and increases osmotic- and salt stress-tolerance of transgenic calli Planta 233 621 634

    • Search Google Scholar
    • Export Citation
  • Poovaiah, B.W., Takezawa, D., An, G. & Han, T.J. 1996 Regulated expression of a calmodulin isoform alters growth and development in potato J. Plant Physiol. 149 553 558

    • Search Google Scholar
    • Export Citation
  • Raices, M., Gargantini, P.R., Chinchilla, D., Crespi, M., Tellez-Inon, M.T. & Ulloa, R.M. 2003 Regulation of CDPK isoforms during tuber development Plant Mol. Biol. 52 1011 1024

    • Search Google Scholar
    • Export Citation
  • Rashotte, A.M. & Goertzen, L.R. 2010 The CRF domain defines cytokinin response factor proteins in plants BMC Plant Biol. 10 74

  • Reddy, A.S.N., Day, I.S., Narasimhulu, S.B., Safadi, F., Reddy, V.S., Golovkin, M. & Harnly, M.J. 2002 Isolation and characterization of a novel calmodulin-binding protein from potato J. Biol. Chem. 277 4206 4214

    • Search Google Scholar
    • Export Citation
  • Ricardo, J. 2011 Screening sweetpotato (Ipomoea batatas L.) for drought tolerance and high β-carotene content. MS thesis, Univ. KwaZulu-Natal, Pietermaritzburg, South Africa

  • Rickard, D.S. & Fitzgerald, P.D. 1969 The estimation and occurrence of agricultural drought J. Hydrol. (Amst.) 8 11 16

  • Riechmann, J.L. & Meyerowitz, E.M. 1998 The AP2/EREBP family of plant transcription factors Biol. Chem. 379 633 646

  • Rus, A., Baxter, I., Muthukumar, B., Gustin, J., Lahner, B., Yakubova, E. & Salt, D.E. 2006 Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis PLoS Genet. 2 e210

    • Search Google Scholar
    • Export Citation
  • Saraswati, P. 2007 Physiological and growth responses of selected sweet potato [Ipomoea batatas (L.) Lam.] cultivars to water stress. PhD diss., James Cook Univ., Townsville City, Australia

  • Schafleitner, R., Tincopa, L.R., Palomino, O., Rossel, G., Robles, R.F., Alagon, R., Rivera, C., Quispe, C., Rojas, L., Pacheco, J.A., Solis, J., Cerna, D., Kim, J.Y., Hou, J. & Simon, R. 2010 A sweetpotato gene index established by de novo assembly of pyrosequencing and Sanger sequences and mining for gene-based microsatellite markers BMC Genomics 11 604

    • Search Google Scholar
    • Export Citation
  • Soderman, E., Hjellström, M., Fahleson, J. & Engstrom, P. 1999 The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions Plant Mol. Biol. 40 1073 1083

    • Search Google Scholar
    • Export Citation
  • Soderman, E., Mattsson, J. & Engstrom, P. 1996 The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid Plant J. 10 375 381

    • Search Google Scholar
    • Export Citation
  • Solis, J. 2012 Genomic approaches to understand sweetpotato root development in relation to abiotic factors. PhD diss., Louisiana State Univ., Baton Rouge, LA

  • Tanaka, M., Kato, N., Nakayama, H., Nakatani, M. & Takahata, Y. 2008 Expression of class I knotted1-like homeobox genes in the storage roots of sweetpotato (Ipomoea batatas) J. Plant Physiol. 165 1726 1735

    • Search Google Scholar
    • Export Citation
  • Togari, Y. 1950 A study of tuberous root formation in sweet potato Bul. Natl. Agr. Expt. Stn. 68 1 96

  • USDA. 2005. United States standards for grades of sweetpotato. 2 Apr. 2014. <http://www.ams.usda.gov/AMSv1.0/getfile?dDocName=STELPRDC5050330>

  • Villordon, A., LaBonte, D. & Solis, J. 2011 Using a scanner-based minirhizotron system to characterize sweetpotato adventitious root development during the initial storage root bulking stage HortScience 46 513 517

    • Search Google Scholar
    • Export Citation
  • Villordon, A.Q., LaBonte, D.R., Firon, N., Kfir, Y., Pressman, E. & Schwartz, A. 2009a Characterization of adventitious root development in sweetpotato HortScience 44 651 655

    • Search Google Scholar
    • Export Citation
  • Villordon, A., LaBonte, D. & Firon, N. 2009b Development of a simple thermal time method for describing the onset of morpho-anatomical features related to sweetpotato storage root formation Sci. Hort. 121 374 377

    • Search Google Scholar
    • Export Citation
  • Villordon, A., Solis, J., LaBonte, D. & Clark, C. 2010 Development of a prototype Bayesian network model representing the relationship between fresh market yield and some agroclimatic variables known to influence storage root initiation in sweetpotato HortScience 45 1167 1177

    • Search Google Scholar
    • Export Citation
  • Xiong, L.M., Schumaker, K.S. & Zhu, J.K. 2002 Cell signaling during cold, drought, and salt stress Plant Cell 14 S165 S183

  • You, M.K., Hur, C.G., Ahn, Y.S., Suh, M.C., Jeong, B.C., Shin, J.S. & Bae, J.M. 2003 Identification of genes possibly related to storage root induction in sweetpotato FEBS Lett. 536 101 105

    • Search Google Scholar
    • Export Citation
  • Rainfall data of Chase, LA, during the experiments of 2010 and 2011 to study the effect of drought stress on storage root yield of sweetpotato (National Oceanic and Atmospheric Administration, 2014).

  • Expression profile of 14 genes in sweetpotato roots from 2-week-old plants under greenhouse drought stress (5 d after transplanting) vs. control by quantitative real-time polymerase chain reaction. Error bars represent sem of two independent experiments averaged over three replications each except IbBEL2, Ibkn2, and IbCRF2, where the se was calculated over the mean of three replicates in a single experiment. Fold change in expression of the genes was determined by normalizing the values against that of the reference gene IbEF1a and calculated relative to the control that was set to 1.0.

  • Albrecht, V., Weinl, S., Blazevic, D., D'Angelo, C., Batistic, O., Kolukisaoglu, U., Bock, R., Schulz, B., Harter, K. & Kudla, J. 2003 The calcium sensor CBL1 integrates plant responses to abiotic stresses Plant J. 36 457 470

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  • Chen, M., Wang, Q.Y., Cheng, X.G., Xu, Z.S., Li, A.C.L., Ye, X.G., Xia, L.Q. & Ma, Y.Z. 2007 GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants Biochem. Biophys. Res. Commun. 353 299 305

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  • Choi, H.I., Hong, J.H., Ha, J.O., Kang, J.Y. & Kim, S.Y. 2000 ABFs, a family of ABA-responsive element binding factors J. Biol. Chem. 275 1723 1730

  • Choi, H.I., Park, H.J., Park, J.H., Kim, S., Im, M.Y., Seo, H.H., Kim, Y.W., Hwang, I. & Kim, S.Y. 2005 Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity Plant Physiol. 139 1750 1761

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  • Constantin, R.J., Hernandez, T.P. & Jones, L.G. 1974 Effects of irrigation and nitrogen fertilization on quality of sweet potatoes J. Amer. Soc. Hort. Sci. 99 308 310

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  • Deng, X., Phillips, J., Meijer, A.H., Salamini, F. & Bartels, D. 2002 Characterization of five novel dehydration-responsive homeodomain leucine zipper genes from the resurrection plant Craterostigma plantagineum Plant Mol. Biol. 49 601 610

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  • de Souza, C.R.B., Carvalho, L. & Cascardo, J.C.D. 2004 Comparative gene expression study to identify genes possibly related to storage root formation in cassava Protein Pept. Lett. 11 577 582

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  • Effendy, J., La Bonte, D. & Baisakh, N. 2013 Identification and expression of skinning injury responsive genes in sweetpotato J. Amer. Soc. Hort. Sci. 138 1 7

    • Search Google Scholar
    • Export Citation
  • Eguchi, T. & Yoshida, S. 2008 Effects of application of sucrose and cytokinin to roots on the formation of tuberous roots in sweetpotato [Ipomoea batatas (L.) Lam.] Plant Root 2 7 13

    • Search Google Scholar
    • Export Citation
  • Ekanayake, I.J. & Dodds, J.H. 1993 In vitro testing for the effects of salt stress on growth and survival of sweetpotato Sci. Hort. 55 239 248

  • Firon, N., LaBonte, D., Villordon, A., Kfir, Y., Solis, J., Lapis, E., Perlman, T.S., Doron-Faigenboim, A., Hetzroni, A., Althan, L. & Nadir, L.A. 2013 Transcriptional profiling of sweetpotato (Ipomoea batatas) roots indicates down-regulation of lignin biosynthesis and up-regulation of starch biosynthesis at an early stage of storage root formation BMC Genomics 14 460

    • Search Google Scholar
    • Export Citation
  • Hjellström, M. 2002 Drought stress signal transduction by the HD-Zip transcription factors ATHB6 and ATHB7. Acta Universitatis Upsaliensis. Comprehensive Summaries Uppsala diss., Faculty Sci. Technol. 690:18

  • Jimenez, J.A., Alonso-Ramirez, A. & Nicolas, C. 2008 Two cDNA clones (FsDhn1 and FsClo1) up-regulated by ABA are involved in drought responses in Fasus sylvatica L. seeds J. Plant Physiol. 165 1798 1807

    • Search Google Scholar
    • Export Citation
  • Kim, S.H., Hamada, T., Otani, M. & Shimada, T. 2005 Isolation and characterization of MADS box genes possibly related to root development in sweetpotato (Ipomoea batatas L. Lam.) J. Plant Biol. 48 387 393

    • Search Google Scholar
    • Export Citation
  • Kim, S.H., Mizuno, K. & Fujimura, T. 2002 Isolation of MADS-box genes from sweet potato [Ipomoea batatas (L.) Lam.] expressed specifically in vegetative tissues Plant Cell Physiol. 43 314 322

    • Search Google Scholar
    • Export Citation
  • Kim, S.H., Song, W.K., Kim, Y.H., Kwon, S.Y., Lee, H.S., Lee, I.C. & Kwak, S.S. 2009 Characterization of full-length enriched expressed sequence tags of dehydration-treated white fibrous roots of sweetpotato BMB Rpt. 42 271 276

    • Search Google Scholar
    • Export Citation
  • Kim, Y.H., Jeong, J.C., Lee, H.S. & Kwak, S.S. 2013 Comparative characterization of sweetpotato antioxidant genes from expressed sequence tags of dehydration-treated fibrous roots under different abiotic stress conditions Mol. Biol. Rpt. 40 2887 2896

    • Search Google Scholar
    • Export Citation
  • Kim, Y.H., Yang, K.S., Ryu, S.H., Kim, K.Y., Song, W.K., Kwon, S.Y., Lee, H.S., Bang, J.W. & Kwak, S.S. 2008 Molecular characterization of a cDNA encoding DRE-binding transcription factor from dehydration-treated fibrous roots of sweetpotato Plant Physiol. Biochem. 46 196 204

    • Search Google Scholar
    • Export Citation
  • Kizis, D., Lumbreras, V. & Pages, M. 2001 Role of AP2/EREBP transcription factors in gene regulation during abiotic stress FEBS Lett. 498 187 189

  • Ku, A.T., Huang, Y.S., Wang, Y.S., Ma, D. & Yeh, K.W. 2008 IbMADS1 (Ipomoea batatas MADS-box 1 gene) is involved in tuberous root initiation in sweet potato (Ipomoea batatas) Ann. Bot. (Lond.) 102 57 67

    • Search Google Scholar
    • Export Citation
  • Lee, Y.H. & Chun, J.Y. 1998 A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment Plant Mol. Biol. 37 377 384

    • Search Google Scholar
    • Export Citation
  • Ley, T.W., Stevens, R.G., Topielec, R.R. & Neibling, W.H. 1994 Soil water monitoring and measurement. Washington State Univ., Pacific Northwest Ext. Publ. 475

  • Lin, R., Zhao, W., Meng, X. & Peng, Y.L. 2007 Molecular cloning and characterization of a rice gene encoding AP2/EREBP-type transcription factor and its expression in response to infection with blast fungus and abiotic stresses Physiol. Mol. Plant Pathol. 70 60 68

    • Search Google Scholar
    • Export Citation
  • Lokko, Y., Anderson, J.V., Rudd, S., Raji, A., Horvath, D., Mikel, M.A., Kim, R., Liu, L., Hernandez, A., Dixon, A.G.O. & Ingelbrecht, I.L. 2007 Characterization of an 18,166 EST dataset for cassava (Manihot esculenta Crantz) enriched for drought-responsive genes Plant Cell Rpt. 26 1605 1618

    • Search Google Scholar
    • Export Citation
  • National Oceanic and Atmospheric Administration 2014 Monthly climatological summary 2010, 2011. 1 Jan. 2014. <http://www.ncdc.noaa.gov/cdo-web/datasets/GHCNDMS/stations/GHCND:USC00169806/detail>

  • Ni, Y.X., Wang, X.L., Li, D.D., Wu, Y.J., Xu, W.L. & Li, X.B. 2008 Novel cotton homeobox gene and its expression profiling in root development and in response to stresses and phytohormones Acta Biochim. Biophys. Sin. (Shanghai) 40 78 84

    • Search Google Scholar
    • Export Citation
  • Noh, S.A., Lee, H.S., Huh, E.J., Huh, G.H., Paek, K.H., Shin, J.S. & Bae, J.M. 2010 SRD1 is involved in the auxin-mediated initial thickening growth of storage root by enhancing proliferation of metaxylem and cambium cells in sweetpotato (Ipomoea batatas) J. Expt. Bot. 61 1337 1349

    • Search Google Scholar
    • Export Citation
  • Olsson, A.S.B., Engstrom, P. & Soderman, E. 2004 The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis Plant Mol. Biol. 55 663 677

    • Search Google Scholar
    • Export Citation
  • Pais, S.M., Garcia, M.N., Tellez-Inon, M.T. & Capiati, D.A. 2010 Protein phosphatases type 2A mediate tuberization signaling in Solanum tuberosum L. leaves Planta 232 37 49

    • Search Google Scholar
    • Export Citation
  • Park, S.C., Kim, Y.H., Jeong, J.C., Kim, C.Y., Lee, H.S., Bang, J.W. & Kwak, S.S. 2011 Sweetpotato late embryogenesis abundant 14 (IbLEA14) gene influences lignification and increases osmotic- and salt stress-tolerance of transgenic calli Planta 233 621 634

    • Search Google Scholar
    • Export Citation
  • Poovaiah, B.W., Takezawa, D., An, G. & Han, T.J. 1996 Regulated expression of a calmodulin isoform alters growth and development in potato J. Plant Physiol. 149 553 558

    • Search Google Scholar
    • Export Citation
  • Raices, M., Gargantini, P.R., Chinchilla, D., Crespi, M., Tellez-Inon, M.T. & Ulloa, R.M. 2003 Regulation of CDPK isoforms during tuber development Plant Mol. Biol. 52 1011 1024

    • Search Google Scholar
    • Export Citation
  • Rashotte, A.M. & Goertzen, L.R. 2010 The CRF domain defines cytokinin response factor proteins in plants BMC Plant Biol. 10 74

  • Reddy, A.S.N., Day, I.S., Narasimhulu, S.B., Safadi, F., Reddy, V.S., Golovkin, M. & Harnly, M.J. 2002 Isolation and characterization of a novel calmodulin-binding protein from potato J. Biol. Chem. 277 4206 4214

    • Search Google Scholar
    • Export Citation
  • Ricardo, J. 2011 Screening sweetpotato (Ipomoea batatas L.) for drought tolerance and high β-carotene content. MS thesis, Univ. KwaZulu-Natal, Pietermaritzburg, South Africa

  • Rickard, D.S. & Fitzgerald, P.D. 1969 The estimation and occurrence of agricultural drought J. Hydrol. (Amst.) 8 11 16

  • Riechmann, J.L. & Meyerowitz, E.M. 1998 The AP2/EREBP family of plant transcription factors Biol. Chem. 379 633 646

  • Rus, A., Baxter, I., Muthukumar, B., Gustin, J., Lahner, B., Yakubova, E. & Salt, D.E. 2006 Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis PLoS Genet. 2 e210

    • Search Google Scholar
    • Export Citation
  • Saraswati, P. 2007 Physiological and growth responses of selected sweet potato [Ipomoea batatas (L.) Lam.] cultivars to water stress. PhD diss., James Cook Univ., Townsville City, Australia

  • Schafleitner, R., Tincopa, L.R., Palomino, O., Rossel, G., Robles, R.F., Alagon, R., Rivera, C., Quispe, C., Rojas, L., Pacheco, J.A., Solis, J., Cerna, D., Kim, J.Y., Hou, J. & Simon, R. 2010 A sweetpotato gene index established by de novo assembly of pyrosequencing and Sanger sequences and mining for gene-based microsatellite markers BMC Genomics 11 604

    • Search Google Scholar
    • Export Citation
  • Soderman, E., Hjellström, M., Fahleson, J. & Engstrom, P. 1999 The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions Plant Mol. Biol. 40 1073 1083

    • Search Google Scholar
    • Export Citation
  • Soderman, E., Mattsson, J. & Engstrom, P. 1996 The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid Plant J. 10 375 381

    • Search Google Scholar
    • Export Citation
  • Solis, J. 2012 Genomic approaches to understand sweetpotato root development in relation to abiotic factors. PhD diss., Louisiana State Univ., Baton Rouge, LA

  • Tanaka, M., Kato, N., Nakayama, H., Nakatani, M. & Takahata, Y. 2008 Expression of class I knotted1-like homeobox genes in the storage roots of sweetpotato (Ipomoea batatas) J. Plant Physiol. 165 1726 1735

    • Search Google Scholar
    • Export Citation
  • Togari, Y. 1950 A study of tuberous root formation in sweet potato Bul. Natl. Agr. Expt. Stn. 68 1 96

  • USDA. 2005. United States standards for grades of sweetpotato. 2 Apr. 2014. <http://www.ams.usda.gov/AMSv1.0/getfile?dDocName=STELPRDC5050330>

  • Villordon, A., LaBonte, D. & Solis, J. 2011 Using a scanner-based minirhizotron system to characterize sweetpotato adventitious root development during the initial storage root bulking stage HortScience 46 513 517

    • Search Google Scholar
    • Export Citation
  • Villordon, A.Q., LaBonte, D.R., Firon, N., Kfir, Y., Pressman, E. & Schwartz, A. 2009a Characterization of adventitious root development in sweetpotato HortScience 44 651 655

    • Search Google Scholar
    • Export Citation
  • Villordon, A., LaBonte, D. & Firon, N. 2009b Development of a simple thermal time method for describing the onset of morpho-anatomical features related to sweetpotato storage root formation Sci. Hort. 121 374 377

    • Search Google Scholar
    • Export Citation
  • Villordon, A., Solis, J., LaBonte, D. & Clark, C. 2010 Development of a prototype Bayesian network model representing the relationship between fresh market yield and some agroclimatic variables known to influence storage root initiation in sweetpotato HortScience 45 1167 1177

    • Search Google Scholar
    • Export Citation
  • Xiong, L.M., Schumaker, K.S. & Zhu, J.K. 2002 Cell signaling during cold, drought, and salt stress Plant Cell 14 S165 S183

  • You, M.K., Hur, C.G., Ahn, Y.S., Suh, M.C., Jeong, B.C., Shin, J.S. & Bae, J.M. 2003 Identification of genes possibly related to storage root induction in sweetpotato FEBS Lett. 536 101 105

    • Search Google Scholar
    • Export Citation
Julio Solis School of Plant, Environmental, and Soil Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA 70803

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Arthur Villordon Sweet Potato Research Station, Louisiana State University Agricultural Center, 130 Sweet Potato Road, Chase, LA 71324

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Niranjan Baisakh School of Plant, Environmental, and Soil Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA 70803

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Don LaBonte School of Plant, Environmental, and Soil Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA 70803

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Nurit Firon Institute of Plant Sciences, The Volcani Center, ARO, P.O. Box 6, Bet Dagan, 50250, Israel

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Contributor Notes

Approved for publication by the Director of the Louisiana Agricultural Experiment Station as manuscript number 2013-306-10779.

Support for this research was provided by a grant from The USA–Israel Binational Agricultural Research and Development grant number US-4015-07.

Corresponding author. E-mail: dlabonte@agcenter.lsu.edu.

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  • Rainfall data of Chase, LA, during the experiments of 2010 and 2011 to study the effect of drought stress on storage root yield of sweetpotato (National Oceanic and Atmospheric Administration, 2014).

  • Expression profile of 14 genes in sweetpotato roots from 2-week-old plants under greenhouse drought stress (5 d after transplanting) vs. control by quantitative real-time polymerase chain reaction. Error bars represent sem of two independent experiments averaged over three replications each except IbBEL2, Ibkn2, and IbCRF2, where the se was calculated over the mean of three replicates in a single experiment. Fold change in expression of the genes was determined by normalizing the values against that of the reference gene IbEF1a and calculated relative to the control that was set to 1.0.

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