Received: 21 July 2019 | Revised: 18 October 2019
DOI: 10.1111/jac.12377
MISCELLANEOUS
Phenological and physiological evaluation of first and second
cropping periods of sorghum and maize crops
Maria Antonia Machado Barbosa
Emilly dos Santos Pereira | Angélica Fátima de Barros | Sebastián Giraldo Montoya |
Leonardo Duarte Pimentel
Department of Plant Science, Federal
University of Viçosa, Viçosa, Brazil
Correspondence
Maria Antonia Machado Barbosa,
Department of Plant Science, Federal
University of Viçosa, Avenida Peter Henri
Rolfs, s/n°, Viçosa, Minas Gerais, Brazil.
Email: mabarbosa483@gmail.com
Funding information
National Council of Scientific and
Technological Development; Brazilian
Federal Agency for Support and Evaluation
of Graduate Education; State of Minas
Gerais Research Foundation; Federal
University of Viçosa
J Agro Crop Sci. 2019;00:1–14.
| Accepted: 22 October 2019
| Kacilda Naomi Kuki | Pedro Santos Peno Bengala |
Abstract
Environmental conditions influence phenology and physiological processes of plants.
It is common for maize and sorghum to be sown at two different periods: the first
cropping (spring/summer) and the second cropping (autumn/winter). The phenologi-
cal cycle of these crops varies greatly according to the planting season, and it is nec-
essary to characterize the growth and development to facilitate the selection of the
species best adapted to the environment. The aim of this study was to characterize
phenological phases and physiological parameters in sorghum and maize plants as a
function of environmental conditions from the first cropping and second cropping
periods. Two parallel experiments were conducted with both crops. The phenological
characterization was based on growth analyses (plant height, leaf area and photoas-
similate partitioning) and gas exchange evaluations (net assimilation rate, stomatal
conductance, transpiration and water‐use efficiency). It was found that the vegeta-
tive stage (VS) for sorghum and maize plants was 7 and 21 days, respectively, longer
when cultivated during the second cropping. In the first cropping, the plants were
taller than in the second cropping, regardless of the crop. The stomatal conductance
of sorghum plants fluctuated in the second cropping during the development period,
while maize plants showed decreasing linear behaviour. Water‐use efficiency in sor-
ghum plants was higher during the second cropping compared with the first crop-
ping. In maize plants, in the second cropping, the water‐use efficiency showed a slight
variation in relation to the first cropping. It was concluded that the environmental
conditions as degree‐days, temperature, photoperiod and pluvial precipitation influ-
ence the phenology and physiology of both crops during the first and the second
cropping periods, specifically cycle duration, plant height, leaf area, net assimilation
rate, stomatal conductance and water‐use efficiency, indicating that both crops re-
spond differentially to environmental changes during the growing season.
KEYWORDS
growing season, growth analysis, phenological phases, Sorghum bicolor, Zea mays
wileyonlinelibrary.com/journal/jac
© 2019 Blackwell Verlag GmbH | 1
2 |
1 | I NTRO D U C TI O N
Plant responses to environmental conditions can vary, depend-
ing on the species and the region of exploitation. Phenology and
physiology are noticeably affected by the environment setting, and
these two processes are closely related to plant productive success
(Brachi, Aimé, Glorieux, Cuguen, & Roux, 2012). Being aware of the
interaction between the environment and phenological and physio-
logical parameters can lead to a better understanding of the growth
and adaptability of the plants to the conditions in which they grow,
besides contributing to correct management and assisting the pro-
ducer in decision‐making during the planting period.
To ensure the farm's grain supply, mainly for animal feed, many
producers have adopted two growing seasons: the first cropping pe-
riod (spring/summer crop) and the second cropping period (autumn/
winter crop) known as the off season (Pacheco et al., 2011). One
of the limiting factors for planting a second cropping is lower rain-
fall, leading to production losses (Dagdelen et al., 2008). Moreover,
out‐of‐season growing impairs crop performance, with reductions in
growth and development arising from physiological and biochemical
changes, such as reduced photosynthetic capacity, enzymatic inacti-
vation and others (Scranton & Amarasekare, 2017).
Some crops are preferably grown during summer and some
during winter. In Brazil, among the crops used for second crop
planting are maize (Zea mays), sorghum (Sorghum bicolor), sunflower
(Helianthus annuus), beans (Phaseolus vulgaris), canola (Brassica
napus), peanuts (Arachis hypogaea), rice (Oryza sativa) and millet
(Pennisetum glaucum). Of these, maize has been adopted as one of
the main succession crops to soya bean planting, playing an import-
ant role in grain production systems (Adegas, Voll, & Gazziero, 2011).
However, factors such as lack of water, for example, have limited the
productive potential of this crop (Kebede et al., 2014).
Maize is the cereal with the largest world production volume,
1,065.1 million t, and 71.4% of world production is concentrated in
the United States, China, Brazil and European Union (Department
of Agribusiness of FIESP, 2017). In the national scenario, maize is
one of the main agricultural crops, being cultivated in all regions of
the country (Artuzo, Foguesatto, Souza, & Silva, 2018). On the other
hand, sorghum has emerged as a good option for second cropping
cultivation, as it has good yields of grain with less water availability
compared with other crops.
Sorghum has been cultivated since the dawn of agriculture and
currently occupies an important place in the world grain market due
to its wide adaptability, versatility and rusticity. This crop is widely
used for animal feed; however, new research indicates its poten-
tial to be inserted in power generation in Brazil (Tang, Li, Li, & Xie,
2018). Individually, some American countries are prominent in sor-
ghum production. The USA leads sorghum production worldwide,
accounting for 16.5% of world production, harvesting 9.88 million
tons. On the African continent, many countries, mainly in the sub‐
Saharan region, are major producers of sorghum, including Nigeria,
Sudan and Ethiopia (EMBRAPA, 2015). Furthermore, its tolerance
MACHADO BARBOSA et al.
towards the lack of water and its good straw yield has led farmers to
opt for it on winter planting compared with maize, showing a great
expansion in its cultivation in grain‐producing regions of Brazil.
For maize, temperature is one of the main factors responsible
for altering its phenology. Moreover, the growth of this crop can
be affected by the lack of water, which is very characteristic during
the second cropping period (Streck, Silva, & Langner, 2012). On the
other hand, sorghum phenology, especially flowering, can be altered
by changes in photoperiod (Buso, Morgado, Silva, & França, 2011).
However, the importance of sorghum and maize to planting systems
and the use of these crops in two annual croppings clearly show
the need for monitoring throughout the cycle depending on envi-
ronmental conditions, helping the producers exploit the productive
potential. To date, there is no information on how the phenology as-
sociated with the physiology of both crops is altered by summer and
winter cultivation. In this context, our hypothesis is that sorghum
and maize plants are influenced by the environmental conditions of
the growing seasons, since they are two crops with different toler-
ances towards changes in water availability, temperature regime and
relative humidity, among others. The purpose of the present study
was to investigate the performance of sorghum and maize plants
under different environmental conditions (first cropping and second
cropping), contributing to a better selection of species during these
growing periods.
2 | M ATE R I A L A N D M E TH O DS
2.1 | Location of the experiment and climatological
evaluations
The study was carried out under field conditions, at the Diogo Alves
of Melo Experimental Station at the Federal University of Viçosa
(UFV), Viçosa, Minas Gerais, Brazil (20°45′14″S and 42°52′53″W).
The experiment started on 25 January 2018 and ended on 17
September 2018, comprising the summer and winter growing sea-
sons in the region. The climate of the region is humid subtropical
(Cwa) according to the Köppen‐Geiger classification. During the ex-
periment, data on rainfall (mm), maximum, average and minimum air
temperature (°C/day) and relative humidity—RH (%; Figure 1a) were
collected at the Main Climatological Station of Viçosa, belonging to
the Department of Agricultural Engineering of UFV. At the same
time, data on Solar Irradiance—SI (MJ/m2) were also obtained in the
climatological season and the vapour‐pressure deficit—VPD (KPa;
Figure 1b) was also calculated based on the data for temperature
and relative humidity of the air, using Jones's formula (1992):
VPDar kPa = 0.61137et × 1 − RH∕100
( ) ( )
where t is calculated by the equation:
( ) ( )
t = 17.502 × Tarec ∕ 240.97 + Tarec
where Tarec is air temperature in °C and RH is relative humidity of the
air in %.
MACHADO BARBOSA et al.
F I G U R E 1 Weekly means for
precipitation, relative humidity
(RH), maximum, minimum and mean
temperatures (a), solar irradiance (SI)
and vapour‐pressure deficit (VPD) (b) in
Viçosa, Minas Gerais, during the months
of January to September 2018. Black
arrows indicate evaluation weeks of the
first cropping, and gray arrows indicate
evaluation weeks of second cropping
2.2 | Fertilizer
The soil was prepared by ploughing it once and harrowing it
twice. The soil in the experiment area is classified as dystrofer-
ric Red‐Yellow Clayey (EMBRAPA, 2013). The chemical prop-
erties of soil are as follows: pH (H2O) = 5.48; p = 62.8 mg/dm3;
K = 139 mg/dm3; Ca2+ = 4.65 cmol c/dm3; Mg 2+ = 1.14 cmol c/dm3;
Al3+ = 0.00 cmol c/dm3; H+ + Al = 4.2 cmol c/dm3; SB = 6.15 cmolc/
dm3; CTC = 10.35 cmol c/dm3; t = 6.15 cmol c/dm3; V = 59.4%; and
P‐Rem = 29.8 mg/L. For the first cropping, 300 kg/ha of N‐P‐K
08‐28‐16 was applied as fertilizer, and for the second cropping,
200 kg/ha of the same formula was applied mechanically at the
time of sowing, using a fertilizer planter. At 30 days after sprouting
each crop, it was also fertilized manually applying to the soil sur-
face 200 kg/ha of urea (90 kg of N) and 150 kg/ha of urea (67.5 kg
of N) in the first cropping and second cropping, respectively.
2.3 | Plant material and sowing
Maize cv. BG7049YH and forage sorghum cv. BRS 658 seeds were
used. Double the number of seeds needed to obtain the desired
stand was used, and each plot was thinned when plants reached
20 cm in height, considering stands of 60.000 plants/ha for maize
and 120.000 plants/ha for sorghum. After thinning, the number of
plants per linear metre was adjusted, being 11 and six plants per lin-
ear metre for sorghum and maize, respectively.
| 3
2.4 | Experiment design
The experiment design was in randomized blocks, with four repli-
cates, and the experimental unit was composed of five plants for
each crop evaluated. Two parallel experiments were conducted: one
for the sorghum crop and the other for the maize crop, and in two
cropping periods (first and second). The treatments consisted of dif-
ferent evaluation periods, counted in days after emergence (DAE),
with 8 evaluations carried out on the first cropping (14, 28, 42, 56,
70, 84, 98 and 112 DAE) and 10 evaluations on the second cropping
(14, 28, 42, 56, 70, 84, 98 and 112, 126 and 140 DAE). The evalu-
ations were made at 14‐day intervals as described by Benincasa
(2003), and the duration of both cultivation periods was 140 days.
In the first cropping, 140 days corresponded to the period of physi-
ological maturation of maize, and in the second cropping, 140 days
were adopted for convenience, due to plants being attacked by birds.
The area of each plot was of 54 m2, with 20 lines of 3 m of length,
and a space of 0.9 m between lines, considering as useful area the
plants in the central metre. The lines evaluated were interspersed
each evaluation period.
2.5 | Phenological and growth characterization
Only the aerial part of the plants was evaluated. For the growth
evaluations, the experimental unit was composed of five plants,
and for measurements of gas exchange, the experimental unit was
4 |
composed of three plants. To define phenological phases, the de-
velopment of sorghum plants was divided into vegetative (VS) and
reproductive (RS) stages, following the pattern adopted for maize,
as proposed by Ritchie, Hanway, and Benson (1993). The pheno-
logical development of each crop in the two growing periods was
monitored weekly for growth leaves and reproductive organs and
recorded with a DSC‐HX1 (Sony®) digital still camera. The vegeta-
tive stages were defined according to the highest leaf of which the
ligule was visible. Changes in developmental stages were consid-
ered when 50% of plants (for each crop) had the same pattern of
development.
The height of the plants was obtained in the field using a tape
measure, measuring from the soil surface to the height of the last
leaf and expressed in metres (m). Then, the plants were manually
harvested by cutting the stem near the soil surface. Leaf area deter-
mination was obtained by detaching all green leaves and measuring
them with area meter model Li‐3100C (Licor) and expressed in cm2.
The dry mass of leaves, stem and panicle/ear were obtained. All veg-
etable material was packed in paper bags and transferred to a forced‐
air ventilation oven with a temperature of 65°C until constant weight
was reached. Weighing was performed using a precision semi‐ana-
®
lytical scale (0.01 g) model UW6200H (Shimadzu ), and values were
expressed in grams (g). From the values of dry mass and leaf area, the
specific leaf area (cm2/g) and partition of assimilates between organs
(%) were calculated, as described by Benincasa (2003).
2.6 | Cumulative degree‐days
The cumulative of degree‐days (CDD °C day) required for the culti-
vation of sorghum and maize in the first and second cropping periods
was determined by the equation proposed by Arnold (1959):
( )
CDD = TM + Tm∕2 −Tb
where CDD = cumulative of degree‐days, °C; TM = maximum tem-
perature of the day, °C; Tm = minimum temperature of the day, °C;
and Tb = lower base temperature, °C. For the sorghum and maize
crops, the Tb was 10°C (Neild & Seeley, 1977; Vila Nova, Pedro
Junior, Pereira, & Ometto, 1972).
2.7 | Gas exchange
Gas exchange measurements were taken on all collection days,
under natural conditions on cloudy days, between 8:00 and 10:00 in
the morning. For every measurement, the first fully expanded leaf of
which the ligule was visible was counted from the apex to the base.
For measurements, an IRGA infrared gas analyser (ACD; model LCPro
SD) with 300 ml/min airflow and coupled light source of 1,000 μmol
photons m −2 −1
s was used. At that time, stomatal conductance (mol
of H2O m−2 s−1), transpiration rate (mmol of H2O m−2 s−1) and net
−2 −1
photosynthesis rate (μmol of CO2 m s ) were measured. Water‐use
efficiency was calculated as the ratio between net assimilation rate
and transpiration.
MACHADO BARBOSA et al.
2.8 | Data analysis
The average data for the two cropping periods were subjected to
variance analysis, with the aid of the R statistical program (R Core
Team, 2014). The effects of the collection days were evaluated
through regression analysis, and the first criterion used to choose
the model was the highest regression coefficient (R 2) considering
the biological interpretation of the parameters. The second cri-
terion was the level of significance (adjusted to 1%, 5% and 10%
probability). The graphs were made using SigmaPlot ® software
version 10.0.
3 | R E S U LT S
In this study, the first cropping experiment was carried out be-
tween January and May 2018, with a cumulative volume of
436 mm of rainfall, mainly concentrated between January and
March. The second cropping (April–September 2018) was char-
acterized as a drier period, registering 119 mm rainfall, with the
greatest accumulation of rainfall in August. Relative humidity
showed little variation during the experimental period, with mean
values of 83% and 82% in the first and second cropping, respec-
tively. Maximum air temperature varied from 23.3 to 31.3°C dur-
ing the first cropping, and during the second varied from 22 to
27.5°C. The minimum air temperature varied between 11.6 and
20°C during the first cropping, and 9.8 and 14.8°C during the sec-
ond. The mean daily temperature varied between 17.8 and 25.4°C
during the first cropping and 20.5 and 16.8°C during the second
(Figure 1a). Mean solar irradiance during the first cropping was
13.8 MJ/m2 , with the highest incidence of 20.4 MJ/m2 recorded
in the second week of February. During the second cropping, the
mean SI was 12.3 MJ/m2 and the highest incidence was 17 MJ/m2 .
VPD, which is an indicator of atmospheric evaporative demand,
reached mean weekly values of 0.07 kPa in the first cropping and
0.09 kPa in the second, with extreme values of 0.04 and 0.13 kPa
in the second week of March and the second week of September,
respectively (Figure 1b).
3.1 | Phenological stages of sorghum and maize
plants are influenced by the first and second
cropping seasons
For sorghum plants, emergence of seedlings occurred 7 days after
sowing, in both cropping periods (Figure 2a). The VS lasted 56 days
in the first cropping, ending with the occurrence of anthesis, while
in the second cropping, this stage lasted 63, 7 days longer. The re-
productive stage (RS) in the first cropping lasted 63 days for sor-
ghum and lasted longer in the second cropping: 77 days. Sorghum
grains reached the degree of physiological maturation (20% grain
moisture) at 112 DAE in the first cropping and 140 DAE in the sec-
ond, representing an increase of 28 days in the crop cycle. For maize
MACHADO BARBOSA et al.
F I G U R E 2 Duration in days of phenological stages (a) and
accumulation of degree‐days—ADD (°C) (b) in sorghum and maize
plants in the first and second cropping in Viçosa, Minas Gerais. E,
emergence; RS, reproductive stage; VS, vegetative stage
plants, emergence also occurred 7 days after sowing in both crop-
ping periods. The duration of VS was 56 and 77 days, for the first and
second cropping, respectively, with an increase of 21 days for the
occurrence of anthesis in plants in the second cropping. The RS oc-
curred when the plants reached stage R6 (30% grain moisture) last-
ing 84 days in the first cropping, and although it was not detected
in the second crop, the plants were in stage R5 at 140 DAE (Table 1,
Figure 2a).
The accumulated degree‐days (ADD) required for emergence
of sorghum and maize plants was 179.8 ADD in the first cropping
and 149.3 in the second (Figure 2b). The ADD accumulation in VS
for sorghum plants in the first cropping was 788.8, while in the sec-
ond cropping, it was 584.6 ADD. In maize plants, VS required 788.8
ADD in the first cropping and 693 ADD during second. The ADD
requirement for sorghum plants in the VS was lower during the first
cropping compared with the second, 630.4 ADD and 653.4 ADD,
respectively. For maize in the first cropping, the VS was 929.8 ADD,
| 5
and in the second, it was not possible to detect the ADD until the
physiological maturity of the plants; however, at 140 days (R5 stage)
the ADD was 545 (Figure 2b).
The change in the vegetative and reproductive development of
sorghum and maize plants in the two growing seasons is shown in
Figures 3 and 4. The difference in days for anthesis in the first and
second cropping in sorghum plants was 7 days and in maize 21 days
(Figure 3). In the RS, phase changes up to 140 days of cultivation can
be noted by changes in the panicle and ear size, and also by grain
coloration (Figure 4).
The height of the sorghum plants cultivated in the first cropping
showed quadratic behaviour (p < .05) as a function of their devel-
opment with a maximum height of 245 cm at 88 DAE. The same
behaviour was evidenced during the second cropping for the same
parameter, with maximum values of 136 cm at 104 DAE (p < .05;
Figure 5a). In maize plants, the maximum height in the first cropping
was 259 cm at 85 DAE (p < .05), while in the second cropping, it was
209 cm at 111 DAE (p < .01; Figure 5b).
Leaf area in sorghum plants reached a maximum value
of 3,525.40 cm2 at 69 DAE in the first cropping (p < .01) and
1,192.12 cm2 at 90 DAE in the second (p < .01). Next, there was
a decrease in the response of this parameter for the two growing
periods (Figure 5c). In maize plants (Figure 5d), maximum leaf area
was obtained at 76 and 88 DAE, with maximum values of 7,173.72
and 4,588.72 cm2 for plants grown in the first and second cropping
periods, respectively (p < .01).
Sorghum and maize plants cultivated in the two cropping periods
showed linear decreasing pattern in specific leaf area throughout
their development (Figure 5e,f). The specific leaf area of the sor-
ghum plants from the first cropping decreased gradually by 1.24 cm2
during the evaluation period (p < .01), while in the second cropping,
this reduction was 1.71 cm2 (p < .01). In maize plants, the daily reduc-
tion in specific leaf area was 1.76 cm2 during the summer (p < .01)
and 0.84 cm2 during the second cropping (p < .01).
Assimilate partitioning between the different organs in sorghum
and maize plant shoots was affected by the growing season (Figure 6).
For sorghum plants cultivated in the first cropping, the decrease in
leaf dry matter allocation was accompanied by an increase in the
dry matter allocation of the stem, which gradually increased up to
70 DAE, with a maximum accumulated amount of 66.92%. From 56
DAE, the panicle contributed to the total dry matter of the plant,
with the metabolic sink shifting to the grains. At the end of the cycle,
the total dry matter of sorghum plants from the first cropping was
9.32%, 47.8% and 42.88%, respectively, for leaves, stem and panicle
(Figure 6a). For sorghum planted in the second cropping, the leaf dry
matter partition was constant until 28 DAE, with a maximum amount
of 70.3%, decreasing after this period. The stem accumulated dry
matter up to 98 DAE (68.6%) and the panicle started to contribute
to total dry matter from 70 DAE, a delay of 14 days in relation to the
period of the first cropping. Assimilate partitioning at the end of the
cycle was 11%, 39% and 50% for leaves, stem and panicle, respec-
tively (Figure 6c).
6 | MACHADO BARBOSA et al.

TA B L E 1 Phenological stages of
Phenological stages
sorghum and maize plants in the first and
Sorghum Maize second cropping (January to September
2018) and evaluated over 140 days
DAE First cropping Second cropping First cropping Second cropping

0 VE VE VE VE
7 V3 V3 V3 V3
14 V4 V4 V5 V4
21 V5 V5 V6 V6
28 V6 V6 V7 V7
35 V8 V7 V8 V7
42 V10 V7 V10 V8
49 V13 V8 V13 V8
56 VT V10 VT V9
63 R1 VT R1 V9
70 R2 R1 R2 V11
77 R2 R2 R3 VT
84 R3 R2 R3 R1
91 R4 R3 R4 R2
98 R4 R3 R4 R2
105 R5 R4 R5 R3
112 R6 R4 R5 R3
119 R4 R5 R4
126 R5 R5 R4
133 R5 R5 R5
140 R6 R6 R5

Note: Phenological stages were described for corn according to Ritchie et al. (1993) and were ap-
plied to sorghum. V indicates vegetative stages, and R indicates reproductive stages.
Abbreviation: DAE, days after emergence.

F I G U R E 3 Characterization of
vegetative and reproductive development
of sorghum and maize plants grown in
the first and second cropping in Viçosa‐
MG. They were evaluated weekly for
140 days following emergence, and the
phenological stage was defined when 50%
of the stand plants presented the same
characteristics. Scale bar = 20 cm

In maize plants grown in the first cropping, the assimilate
partitioning of the leaves reduced as the plants developed. This
occurred at the same time as the accumulation of dry matter of
the stem increased up to 56 DAE, and the maximum amount ac-
cumulated in relation to the total dry matter was 53.94%. After
said period, reproductive phase began, with a decrease in the dry
matter accumulated in the stem and an increase in the partition to
the ear, to the detriment of the change in the preferential drain. At
the end of the evaluation period, the total dry matter distribution
was 12.2%, 25.9% and 61.9% for leaves, stem and ear, respectively
MACHADO BARBOSA et al.
F I G U R E 4 Representation of
the reproductive organs of sorghum
and maize plants grown during the
first and second croppings counted
from pollination. The change in the
development of the grains up to 140 days
of cultivation can be noted by the change
in the size of the panicles and ears and in
the coloring of the grains
(Figure 6b). Assimilate partitioning for leaves in maize in the second
cropping increased up to 28 DAE, with maximum share of 72.3%
of total dry matter of the plant in this period. From this period, the
dry matter of the stem increased up to 84 DAE, with a subsequent
decrease due to the beginning of the ear development, which con-
tributed to total dry matter of the plant with a delay of 28 days
compared with the planting of first cropping. In the end, the total
dry matter was represented by 14.8% for leaves, 26.2% for stem
and 58.9% for ear (Figure 6d).
3.2 | The growing season promoted changes in the
gas exchange and water‐use efficiency differently in
sorghum and maize plants
Sorghum plants showed quadratic behaviour for net assimilation
rate during the first and second cropping periods (p < .05), with
maximum values of 36.5 and 22.1 µmol m−2 s−1, respectively
(Figure 7a). During the first cropping, the net assimilation rate of
the maize plants showed quadratic behaviour, with a maximum
value of 38.2 µmol m−2 s−1 at 26 DAE (p < .05). During the second
cropping, the net assimilation rate showed negative linear behav-
iour (p < .01), with a gradual reduction of 0.08 µmol m−2 s−1 over
the period evaluated, from the maximum value of 27.3 µmol m−2 s−1
(Figure 7b).
Stomatal conductance was significantly reduced in sorghum
plants as a function of the collection days when cultivated in the
first cropping (p < .01). This reduction was 0.002 mol m−2 s−2 daily. In
sorghum cultivated in the second cropping, the values for stomatal
conductance oscillated throughout the development of the plants,
| 7
characteristic of the cubic model (p < .1), the lowest value being
0.115 mol m−2 s−1 at 14 DAE and the highest 0.218 mol m−2 s−1 at 56
DAE (Figure 7c). In maize plants, stomatal conductance showed neg-
ative linear behaviour during the first cropping season (p < .01) with
a reduction of 0.003 mol m−2 s−1 daily. In the second cropping, there
was also negative linear behaviour (p < .01), with daily decreases of
0.0005 mol m−2 s−1 (Figure 7d).
The transpiration rate of sorghum plants adjusted itself to a qua-
dratic model in the two growing seasons. At 46 DAE, the sorghum
plants in the first cropping showed a maximum transpiration value
of 3.48 mmol m−2 s−1 (p < .05). In the second cropping, although no
major variations were observed in this parameter, at 96 DAE there
was a maximum transpiration of 1.94 mmol m−2 s−1 (p < .1; Figure 7e).
In maize plants in the first cropping, the maximum transpiration was
4.05 mmol m−2 s−1, verified at 46 DAE. During the second cropping,
maximum transpiration was verified at 57 DAE, with mean values of
2.1 mmol m−2 s−1 (Figure 7f).
During the development of the sorghum plants in the first
cropping, water‐use efficiency varied throughout the evalua-
tion period and was statistically represented by cubic behaviour
(p < .05), starting from values of 13.2 µmol/mol and reaching final
values of 6.96 µmol/mol. In the second cropping, water‐use effi-
ciency showed a decreasing linear trend (p < .05), with a gradual
reduction of 0.03 µmol/mol starting from values of 15.6 µmol/
mol (Figure 8a). In maize plants, water‐use efficiency followed
cubic pattern in the first cropping (p < .05), with intense variations
throughout the crop cycle, presenting initial values of 13.2 µmol/
mol and final values of 7.48 µmol/mol. During the second crop-
ping, a decreasing linear trend (p < .05) was observed, with a
8 | MACHADO BARBOSA et al.

F I G U R E 5 Plant height (a and b), leaf area (c and d) and specific leaf area (e and f) in sorghum and maize plants, depending on the
evaluation period (days after emergence) and first cropping (●) and second cropping (□) in Viçosa, Minas Gerais. Each symbol represents the
mean value of 20 sub‐samples and 4 replicates. The symbols: ***, ** and * indicate the significance levels of 1%, 5% and 10% of probability,
respectively

gradual decrease of 0.02 µmol/mol over the period and with initial
values of 12.95 µmol/mol (Figure 8b).
4 | D I S CU S S I O N
Environmental conditions during the cultivation period are essential
to the productive success of the plants. Sorghum and maize have
C4 metabolism, which gives them greater potential in the use of
atmospheric carbon (CO2), solar irradiance and water (Way, Katul,
Manzoni, & Vico, 2014). However, they are plants with different
responses and tolerances when the supply of resources becomes
limited. In this study, it was observed that during the second crop-
ping, there were reductions in rainfall volume, solar irradiance and
air temperature, as well as an increase in VPD (Figure 1a,b), while the
length of the day was also reduced. These environmental changes
influenced the phenological stages of both crops studied, such as
prolongation in the VS and delays in the RS. These results were more
pronounced in maize plants, which had a significant prolongation in
VS and RS (Table 1, Figures 4, 5 and 6). Sorghum plants are known
MACHADO BARBOSA et al.
F I G U R E 6 Partition of assimilates for the different organs of the aerial part, in sorghum (a and c) and maize (b and d) plants, according to
the evaluation period (days after emergence) and first and second cropping in Viçosa, Minas Gerais
for showing greater tolerance to extreme conditions compared with
other cereals, with temperature requirement for optimal growth and
development ranging between 27 and 30°C (Hasan, Rabei, Nada, &
Abogadallah, 2017). For maize plants, this requirement is from 24 to
30°C with a strong correlation between the number of accumulated
leaves and the temperature (Clerget, Dingkuhn, Gozé, Rattunde, &
Ney, 2008). Maulana and Tesso (2013), evaluating the influence of
low temperatures in phenological stages of sorghum, did not ob-
serve negative effects on seedling stage, but only a delay in flower-
ing and grain maturity. Kefale and Ranamukhaarachchi (2004) also
observed a prolongation in the vegetative and reproductive stages
of maize plants due to lower soil water availability, which is in agree-
ment with our results.
Air temperature is one of the main factors reflected in the crop
cycle, with the number of hours of heat per day being a determinant
for the phenological stages (Borghi et al., 2017). For most species,
the ADD requirement in the vegetative stage is higher than in the re-
productive stage (Hatfield & Prueger, 2015). This was found only for
sorghum plants grown in the first cropping and not for maize plants.
However, the ADD requirement during the second cropping was
| 9
lower in all stages, for both sorghum and maize (Figure 4b). These re-
sults may be associated with the lower temperatures recorded in this
period, requiring the plants to remain in the field longer to complete
their cycle (Prela & Ribeiro, 2002).
In this study, it was observed that the beginning of the RS of
the sorghum did not undergo major alterations in the second crop-
ping in relation to the ones from the first, but maize showed a longer
delay, both for the beginning of the stage and for the maturation
of the grains (Figure 4). Considering the cultivation period and the
location of our experiments (latitude above 15°), the photoperiod
of the second cropping was shorter in relation to the first cropping
(Rubim, Nascimento, & Morellato, 2010); that is, the shorter days
may have been associated with the increase in cycle length in both
crops. Moreover, lower temperatures in the second cropping period
may be a factor contributing most to the delay in flowering of both
crops, due to its intimated relation with metabolism (Maulana &
Tesso, 2013). Kapanigowda et al. (2013) evaluating different planting
times on agronomic traits of different sorghum lines and hybrids ob-
served a delay of 12 days in flowering, which is associated with lower
temperatures of the period, recorded with averages of 14°C. These
10 | MACHADO BARBOSA et al.

F I G U R E 7 Net assimilation rate (a and b), stomatal conductance (c and d) and transpiration rate (e and f) in sorghum and maize plants,
as a function of the evaluation period (days after emergence) and first cropping (●) and second cropping (□) in Viçosa, Minas Gerais. Each
symbol represents the mean value of 20 sub‐samples and four replicates. The symbols: ***, ** and * indicate significance levels of 1%, 5% and
10% of probability, respectively

results corroborate our results and also confirm the effects of low
temperatures on the cycle of these crops. Delays in flowering and
grain maturity time were also observed for maize plants in the sec-
ond cropping, which is mainly explained by the photoperiod change
(Bonelli, Monzon, Cerrudo, Rizzalli, & Andrade, 2016).
Plants grown under ideal conditions show normal growth and
development; however, when conditions become more extreme,
such as decreases in rainfall, solar irradiance and temperature, for
example, metabolic and physiological processes can be altered,
impacting growth (Anjum et al., 2011; Chinnusamy, Zhu, & Zhu,
2007). Our results show that plant height, leaf area and specific
leaf area in both crops were lower in the second cropping period
(Figure 5). In maize plants, the possible causes of plant height re-
ductions may include the temperature factor, which is already well
known for reducing growth, and consequently productivity, in
these plants (Rymen et al., 2007). For sorghum, there is also sensi-
tivity to the photoperiod, which leads to decreases in plant height
(Wolabu & Tadege, 2016). Moreover, the final height of the plants
is strongly correlated with the length and number of internodes,
and these can be reduced by lower water availability, a situation
that actually occurred in the second cropping (Fujii, Nakamura, &
Goto, 2014; Yamamoto, Guo, & Ninomiya, 2016). Boomsma et al.
MACHADO BARBOSA et al.
F I G U R E 8 Water use Efficiency (a and b) in sorghum and maize
plants, according to the evaluation period (days after emergence)
and planting of the first cropping (●) and second cropping (□) in
Viçosa, Minas Gerais. Each symbol represents the mean value of 20
sub‐samples and 4 replicates. The symbols: ***, ** and * represent
significance levels of 1%, 5% and 10% probability, respectively
(2010) evaluated a long‐term continuous planting of maize, ob-
serving that year‐over‐year environmental changes will lead to
reductions in plant heights due to lower temperatures and soil
moisture.
Leaf area of sorghum and maize plants was impacted during
the second cropping compared to the first one. Although leaf area
of sorghum plants was lower under the second cropping condi-
tions, this parameter was almost constant from the beginning to
the end of the phenological stages, which may be associated with
the ability of sorghum plants to stay green, ensuring photosynthe-
sis in the leaves under conditions of water shortage (Borrell et al.,
2014). More limiting resource conditions promote the reduction in
leaf area, as well as the genetic aspects of the plant itself (Fender,
Mantilla‐Contreras, & Leuschner, 2011). Factors such as soil and
air temperature and especially soil moisture are determinant in
| 11
leaf expansion. Although this study did not evaluate soil moisture,
the extended lower levels of rainfall in the second cropping pe-
riod suggest that field soil capacity was lower, and consequently,
this reflected in the leaf area, since water is fundamental for the
maintenance of cellular expansion and turgor (Kim, Stumpf, Sung,
& Lee, 2018). Additionally, leaf growth may further be reduced by
alteration in membrane transport processes which are tempera-
ture dependent (van Volkenburgh, 1999). Reductions in leaf area
were also reported by Kakani, Vu, Allen, and Boote (2011) when
working with sorghum and maize plants under low soil moisture
condition, confirming the results obtained in our study.
The lowest values of specific leaf area in response to the second
cropping period may be associated with reductions in leaf dry mass
(see Figure 6) throughout the development of sorghum and maize
plants (Amanullah, 2015). Other studies have also highlighted the
reduction in specific leaf area with advancing plant age (Nouvellon et
al., 2010), being in accordance with our results. Moreover, not only
ontogenetic factors (leaf and plant age) but also several environmen-
tal factors, such as restriction of water, light and nutrients, can affect
specific leaf area (Karavin, 2013).
The lower availability of resources in the second cropping
caused a delay of about 14 days, so that the dry matter of the
panicle contributed to the total dry matter in sorghum plants. In
maize plants, this delay was even longer, 28 days compared to the
first cropping (Figure 6). These results are a reflection of delays
in the reproductive stage of both crops in the second cropping
period, especially in maize. During plant development, the demand
for photoassimilates increases due to the growth and formation of
new organs, and in this process, the sugars formed in the source
tissues are directed to other parts of the plant, such as the stem,
roots and fruits (Anuradha & Bishnoi, 2017). In this case, the ef-
fects of the environment on these processes can be significant; for
example, water deficit and low nocturnal temperatures diminish
translocation by increasing the viscosity of the phloem solution
(Guardiola & García‐Luis, 1993). Thus, the adaptability of the plant
in the stressful environment can contribute to partitioning of the
assimilated carbon and consequently improve the development
of the crop. These results are congruent with previous reports in
maize plants, which demonstrated that a lower soil moisture leads
to a reduction in biomass accumulation in reproductive stage (Ge,
Sui, Bai, Tong, & Sun, 2012).
The net assimilation rate of sorghum and maize plants during
the second cropping period was similar, showing the highest rates
in the initial period of development, with reductions following
the same behaviour as the decrease in the leaf area (Acciaresi &
Guiamet, 2010). Environmental conditions in the winter period
were preponderant so that net assimilation rate was lower than in
the first cropping for both crops (Figure 7a,b). Low temperatures
may have promoted inhibition in chloroplast function, altering the
composition of foliar pigments (Maulana & Tesso, 2013), as well
as lower levels of solar irradiance and water availability, especially
during vegetative growth (Righi et al., 2007). Increases in VPD val-
ues, as well as low rainfall levels, probably drove the reduction
12 | MACHADO BARBOSA et al.
in stomatal conductance, affecting the diffusion of CO2 into the
leaf, leading to decreases in net assimilation rate (Grossiord et al.,
2017). In general, reductions in net assimilation rate during plant
growth after full leaf expansion occur, and this decline is generally
driven by a decrease in stomatal conductance and transpiration
rates (Locke & Ort, 2014). It is possible that sorghum plants have
more efficient strategies to cope with winter growing conditions,
keeping stomatal conductance relatively stable during the vege-
tative stage (Figure 7c,d), contributing to the net assimilation rate
values found (Ocheltree, Nippert, Kirkham, & Prasad, 2014). A de-
crease in net assimilation rate values as a result of increases in
VPD values has also been reported in maize (Vitale et al., 2011)
and sorghum (Fracasso, Trindade, & Amaducci, 2016) plants, con-
firming the results of this study.
Stomatal closure is considered a mechanism to prevent dehy-
dration in plants in periods of low rainfall by reducing transpiration
rates, and it is already well known that sorghum plants have good
stomatal control in an attempt to reduce water losses in critical pe-
riods (Benešová et al., 2012). Interestingly, our results in the second
cropping showed that although stomatal conductance values in the
vegetative stage were higher in sorghum plants than in maize, this
did not translate into higher transpiration rates (Figure 7e,f), con-
tributing to the water‐use efficiency values recorded at this stage. In
maize plants, the reduction in stomatal conductance in the second
cropping was constant during plant development, as well as that of
net photosynthesis rate, showing that the performance of physio-
logical processes in this crop is more influenced under a stressful
environment (El‐Sabagh, Barutcular, & Islam, 2017). Reductions in
stomatal conductance were observed in maize and sorghum plants
during the pre‐ and post‐flowering dehydration, confirming our re-
sults (Takele & Farrant, 2013).
The physiological changes caused by the ageing of foliar tissues
contribute to a reduction in water loss rates during plant develop-
ment, which has an intrinsic relationship with the transpiration of
plants (Tardieu, 2013). In fact, lower transpiration values may be in-
teresting for plants in drought conditions, as they prevent water loss
and ensure a higher degree of hydration to plant tissues, and con-
sequently greater water‐use efficiency (Gajanayake & Reddy, 2016).
Plants with lower transpiration values for the same photosynthesis
value are more efficient in water use and have greater tolerance to
drought (Hepworth, Doheny‐Adams, Hunt, Cameron, & Gray, 2015).
Our results show that the water‐use efficiency increased in the
second cropping period compared with the first in both crops stud-
ied (Figure 8a,b). Better performance in this parameter in sorghum
plants confirms that this cereal is well adapted to situations of low
water supply, using available water more efficiently in its metabolic
processes (Ajeigbe, Akinseye, Ayuba, & Jonah, 2018). Increases in
water‐use efficiency were observed in sorghum biomass (Enciso,
Jifon, Ribera, Zapata, & Ganjegunte, 2015), saccharine sorghum
(Curt, Fernandez, & Martinez, 1995) and grain sorghum (Jabereldar,
Naim, Abdalla, & Dagash, 2017) in conditions of low water availabil-
ity. Moreover, Hasan et al. (2017), evaluating the responses of sor-
ghum and maize plants to water deficit, observed a lower tolerance
to drought in maize plants, which presented a lower water‐use effi-
ciency, as well as greater growth reductions, relative leaf water con-
tent and gas exchange.
In conclusion, the environmental conditions as ADD, tempera-
ture, photoperiod and pluvial precipitation during the second crop-
ping period influenced the phenology and physiology of both crops,
specifically cycle duration, plant height, leaf area, net assimilation
rate, stomatal conductance and water‐use efficiency. In the second
cropping period, the VS in the 7 day for sorghum and in the 21 day
for maize increased, due to lower temperatures. In addition, the time
grain maturity delayed, at 140 DAE, the sorghum plants were in R6
and the maize plants were in R5. The conditions during the second
cropping (low temperature and shortest photoperiod, specially) led
to a decrease in leaf area and specific leaf area, and this result is
more significant in maize plants, contributing to a lower performance
of gas exchange in this crop. Furthermore, our results showed that
water‐use efficiency increased during the second cropping, espe-
cially for sorghum plants, due to less rainfall, reaffirming the higher
tolerance of this cereal under conditions of water deficit.
AC K N OW L E D G E M E N T S
“This study was financed in part by Brazilian Federal Agency for
Support and Evaluation of Graduate Education (CAPES)—Finance
Code 001,” by the State of Minas Gerais Research Foundation
(FAPEMIG/Brazil), National Council of Scientific and Technological
Development (CNPq/Brazil) and the Federal University of Viçosa
(UFV/Brazil).
C O N FL I C T O F I N T E R E S T
The authors declare that they have no conflicts of interest.
AU T H O R S ' C O N T R I B U T I O N
LDP was the supervisor of this project, planning all stages of this
research. MAMB conducted the experiments in the field, collected
and interpreted the data and writing the manuscript. KNK and SGM
contributed to interpretation of the data and writing the manuscript.
PSB, ESP and AFB assisted in conducting the experiment and pheno-
logical and physiological determinations.
ORCID
Maria Antonia Machado Barbosa https://orcid.
org/0000-0002-8701-0599
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How to cite this article: Barbosa MAM, Kuki KN, Bengala PSP,
et al. Phenological and physiological evaluation of first and
second cropping periods of sorghum and maize crops. J Agro
Crop Sci. 2019;00:1–14. https​://doi.org/10.1111/jac.12377​