Nativa, Sinop, v. 10, n. 2, p. 142-153, 2022.
Pesquisas Agrárias e Ambientais
DOI: https://doi.org/10.31413/nativa.v10i2.13078 ISSN: 2318-7670
Effects of droughts on carbon allocation in plants
Angélica Alves GOMES1, Andréa Carvalho da SILVA1*
1 Postgraduate Program in Agronomy, Federal University of Mato Grosso, Sinop, MT, Brazil.
*E-mail: andrea.silva@ufmt.br
(ORCID: 0000-0002-8966-2187; 0000-0003-2921-3379)
Recebido em 13/10/2021; Aceito em 09/03/2022; Publicado em 03/06/2022.
ABSTRACT: The objective of this review was to gather information about the effects of droughts on the
allocation of carbon in plants. Plants are sessile organisms; thus, they are continuously exposed to
environmental changes, mainly, those related to climate. Water is the most important climate factor. Rainfall
variations and poor rainfall distribution can result in drought conditions, affecting negatively essential processes
in plants, such as photosynthesis. This review presents, in a summarized form, some responses of plants to
drought conditions and the effects of droughts on the process of carbon allocation, which makes evident that
the nature and intensity of its effects are variable and dependent on the species, ontogeny, and level of sensitivity
of the plant to water stress.
Keywords: carbon balance; water deficit; photoassimilates; carbohydrates.
Efeitos da seca na alocação de carbono nos vegetais
RESUMO: Objetivou-se com esta revisão, levantar informações sobre os efeitos da “seca” no padrão de
alocação de carbono nos vegetais. Por serem organismos sésseis, estão continuamente expostos as mudanças
ambientais, principalmente a nível de clima. Dentre os fatores climáticos, a água é considerada o mais
importante. As variações pluviométricas, e a má distribuição podem vir a ocasionar condições de seca, afetando
negativamente processos essenciais como a fotossíntese. Nesta revisão, são apresentadas de forma resumida,
algumas respostas dos vegetais frente as condições de seca, e a interferência desta no processo de alocação de
carbono, ficando evidente que, a natureza e intensidade de interferência é variável, sendo determinada pela
espécie, ontogenia e nível de sensibilidade ao estresse.
Palavras-chave: balanço de carbono; déficit hídrico; fotoassimilados; carboidratos.
1. INTRODUCTION
Plants are sessile organisms that are continuously exposed
to environmental changes that threaten their survival, mainly
those connected to climate. Water is among the most limiting
climate factors to development and growth of plants.
Water availability can be limited by droughts, high
salinity, and freezing; it is one of the main risk factors for
plant production in natural and agricultural habitats. In this
review, water availability is treated as result of conditions of
drought, which refers to meteorological conditions
commonly connected to periods of low or no rainfall that
result in soil water deficit. In plants, droughts cause losses of
water in their tissues and cells.
Considering the current situation of intense climatic
variations over short periods, it is expected that extreme
events, such as droughts, occur with high frequency and
intensity, affecting the future climate and impacting the
carbon (C) balance of ecosystems.
Considering the importance of water for agriculture, the
effects of droughts on development of plants have been
widely studied, focused on identifying physiological and
molecular responses activated by plants under water
limitations.
Some already identified responses include life cycle
changes, phenotypic changes in leaf structure and
development (REGIER et al., 2009), changes in root to shoot
growth ratio (ANDEREGG, 2012), regulation of opening
and closure of stomata (RUEHR et al., 2009), accumulation
of solutes (PEREIRA et al., 2012; MONTEIRO et al., 2014),
strategies for detox of reactive oxygen species, and metabolic
changes (CHAKRABORTY; PRADHAN, 2012;
MAGALHÃES et al., 2016).
These responses are affected by C allocation, which refers
to regulation of distribution of the assimilated C in the
storage organ (leaf) for metabolism and transport as starch
and sugars (HASIBEDER et al., 2015; TAIZ et al., 2017).
Therefore, predicting responses of plants to
environmental changes and the consequences for the
ecosystem functioning requires understanding the regulation
of the C allocation process; thus, the objective of this work
was to gather information on the effects of droughts on C
allocation in plants.
2. LITERATURE REVIEW
2.1. Definition of drought and its implications
Drought is a meteorological term commonly connected
to periods of low or no rainfall that result in water deficit. In
the soil, drought is the result of several factors, such as strong
evaporation resulting from a high evaporative demand of
atmosphere caused by high radiation levels and high
temperatures; Moreover, high salinity and freezing of soils
reduce water availability, causing water stress in plants
(Figure 1). In plants, droughts cause loss of water in tissues
and cells (WOOD, 2005).
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Nativa, Sinop, v. 10, n. 2, p. 142-153, 2022.
143
Figure 1. Water stress as result of interaction between climate
factors.
Figura 1. Estresse hídrico como resultado da interação entre fatores
climáticos.
A drought can be quantified, standardized, and compared
through indicators. The Standardized Precipitation Index
(SPI) developed by Mckee; Doesken; Kleist, (1993) is among
the indicators that have been increasingly used worldwide
and is considered as one of the most updated for quantifying
rainfall excess or water deficit in different time scales. SPI
classifies droughts into classes, namely: light, moderate,
severe, and extreme, which are also adopted for rainy periods
(MCKEE et al., 1993).
In general, the water that entries and flows through a
plant body is from the soil, and the force that drives this entry
is dependent on the existence of a decreasing gradient of
water potential (Ψw); in normal water availability conditions,
the soil presents higher Ψw than the atmosphere, and the
water exchange to the atmosphere is mediated by plants that
work as a conductor.
Water deficit promoted by drought conditions prevents
water exchanges in the soil-plant-atmosphere system, and it
is considered as one of the most limiting abiotic factors to
establishment, growth, and development of plants in most
natural and agricultural habitats. The primary effects of this
condition are expressed by decrease of Ψw in the soil, plant,
and atmosphere, cell dehydration, and increase in water
resistance (TAIZ et al, 2017).
There are several classifications for sensitivity to water
stress, and the intensity of the effects caused by stress is
connected to the sensitivity level and capacity of adaptation
or acclimatization of plants, which enable them to survive
and recover.
The adaptation to the environment is characterized by
genetic changes in the whole population, fixed by natural
selection during many generations, whereas acclimatization is
a result of phenotypic plasticity, which corresponds to single
and specific non-permanent changes in the plant physiology
or morphology that result in ability to survive and develop in
different environments and can be reverted in case of
changes in the environmental conditions (VALLADARES et
al., 2016).
Adaptation mechanisms and acclimatization of plants
that allow them to thrive in drought conditions classify them
into the categories: plants that delay, escape, or tolerate
dehydration (BEWLEY, 1979). Plants that delay dehydration
can keep their tissues hydrated by increasing their Ψw; plants
that escape from droughts can short their cycle, completing
their vegetative and reproduction stages when water is still
available in the environment; and plants that tolerate
dehydration keep their metabolism even under conditions of
low Ψw (WOOD, 2005; KOOYERS, 2015).
Mechanisms of delay, escape, and tolerance as response
to soil water availability can be expressed through changes in
the life cycle, phenotypic changes in the leaf structure and
dynamics (REGIER et al., 2009), changes in the root to shoot
growth ratio (ANDEREGG, 2012), regulation of stomatal
opening and closure (RUEHR et al., 2009), accumulation of
solutes (PEREIRA et al., 2012; MONTEIRO et al., 2014),
strategies for detox of reactive oxygen species, and metabolic
changes (CHAKRABORTY; PRADHAN, 2012;
MAGALHÃES et al., 2016).
The amount of available water in the soil that is required
for implementation, growth, development, and production
of plants varies according to the species; the critical limit of
available water is associated to the emergence of visible signs
of injury and disturbances in a specific function in the plant.
Soil water balance can be assessed through indicators, such
as relative water content, water potential (Ψw), and osmotic
potential (Ψs) (MONTEIRO et al., 2014; NASCIMENTO et
al., 2019), which also indicate the plant water balance.
Ψw was used to represent the water balance of plants
under drought conditions and its effects on physiological
processes (Figure 2), and the soil Ψw was used to characterize
the drought for some plant species under experimental
conditions (Table 1). The Ψw results found denote a
variation in sensitivity, according to the species and growing
sites.
Table 1 shows that the species Bowdichia virgilioides
tolerates a higher drought level than the others studied. The
differences in Ψw between environments of open vegetation
and Cerrado forest are mainly due to the type of vegetation.
The highest Ψw found for the Cerrado forest is explained by
a little presence of grass species and a high occurrence of
shading, which decrease the water consumption and loss in
the environment; this environmental condition is
characteristic of a high sensitivity of the species, denoting an
adaptation to the open vegetation environment, as the
drought condition for the species in this environment
expressed lower Ψw than that in the Cerrado forest.
Regarding the dynamics of plants in relation to water loss
and the control mechanisms involved, the species are
classified as isohydric and anisohydric. Maize is among the
isohydric species that exhibit changes in stomatal
conductance as a function of the soil water status before
presenting any substantial change in leaf water potential, and
the water loss is regulated by chemical products, such as
abscisic acid (ABA) (hydro-active control) and water
signaling (hydro-passive control). Sunflower is an example of
anisohydric plant, presenting water loss control with lower
contribution of hydro-passive signaling. Both water loss
controls are mechanisms triggered by water deficit and are
the first short-term feedback process in stress and high
evaporative demand conditions (TARDIEU et al., 2018).
Five short-term feedback processes can be considered for
control of water loss in plants: the first are hydro-active and
hydro-passive; the second are changes in water conductance
in tissues, attenuating fast changes in water potential, thus
assisting to maintain water uptake in dry soils; the third is a
fast osmotic adjustment (MONTEIRO et al., 2014); the fourth
is a decrease in leaf area expansion, which decreases losses by
evapotranspiration with effects on root growth, leading to an
increase in the root to shoot ratio, stabilizing the leaf water
status (ANDEREGG, 2012; DURAND et al., 2016); the fifth
is the optimization of carbon to the water status, since in dry
soil conditions, the expansive growth of plants is affected
Effects of droughts on carbon allocation in plants
Nativa, Sinop, v. 10, n. 2, p. 142-153, 2022.
144
earlier and more intensively than the photosynthesis due to a
high resilience of the photosynthetic apparatus to water
deficit; therefore, plants under stress tend to present excess
carbon in the source (SALMON et al., 2019).
Figure 2. Simplified conceptual model of effects of drought in leaf, phloem, and root physiological processes, driven by reductions in water
potential (left) and hypothetical physiological changes as the drought (right) progresses. (+) and (-) represent individual effect of each arrow;
areas in light, medium, and dark gray represent light, moderate, and severe drought, respectively; continuous lines represent well-established
relationships, and dashed lines represent speculative relationships. Source: Adapted from Salmon et al. (2019). Cerrado forest = forest
formation, with tree cover of 50% to 90%; open vegetation = predominantly herbaceous-shrubby vegetation, occurring in shallow or deep
soils with low fertility.
Figura 2. Modelo conceitual simplificado dos efeitos da seca em processo fisiológicos da folha, floema e raiz, impulsionados pela redução
do potencial hídrico (esquerda) e mudanças fisiológicas hipotéticas com a progressão da seca (direita). Sinais de (+) e (-) simbolizam o efeito
individual de cada seta, áreas em cinza claro, médio e escuro representam seca leve, moderada e severa respectivamente, linhas contínuas
representam relações bem estabelecidas e linhas tracejadas relações especulativas, tons de cinza Fonte: Adaptado de Salmon et al. (2019).
Cerradão = formação florestal, com cobertura arbórea variando de 50 a 90%; campo sujo = vegetação predominantemente herbácea-
arbustiva, de ocorrência em solos rasos ou profundos de baixa fertilidade.
Table 1. Water potential (Ψw) in the soil, characterizing water stress conditions in experimental situations for different species and growing
sites.
Tabela 1. Potencial hídrico (Ψw) do solo caracterizando condições de estresse hídrico em situações experimentais para diferentes espécies
e locais de crescimento.
Species Growing site
Experimental
conditions
Soil Ψw
(Mpa) References
Sucupira-do-cerrado (Bowdichia
virgilioides) Cerrado biome, Brazil
(tropical seasonal) Open
vegetation -6.2 (KANEGAE et al., 2000)
Sucupira-do-cerrado (Bowdichia
virgilioides) Cerrado biome, Brazil
(tropical seasonal) Cerrado forest -2.8 (KANEGAE et al., 2000)
Alamo negro (Populus nigra, Poli) Southern Italy (hot
and temperate) Pots -0.01 (REGIER et al., 2009)
Alamo
negro (
Populus nigra,
58
-
861)
Northern Italy (cold
and temperate) Pots -0.02 (REGIER et al., 2009)
Autotetraploid rice (Oryza sativa)
Northern China
(subtropical wet) Pots -0.02 (YANG et al., 2014)
Diploid rice (Oryza sativa)
Northern China
(subtropical wet) Pots -0.04 (YANG et al., 2014)
Sorghum (Sorghum bicolor)
Central Minas Gerais
state, Brazil (tropical) Pots -0.1 (MAGALHÃES et al., 2016)
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145
Plants may also present long-term feedback processes,
which include intrinsic properties for optimization of water
resources over time, such as changes in cycle duration and
phenology; abortion of grains, resulting in lower quantity, but
more viable grains; root system architecture; deeper root
systems with less lateral roots; leaves with the ability to
maintain photosynthetic functions and delay senescence
(Stay-Green phenotype) (TARDIEU et al., 2018).
2.2. Photosynthesis - primary process of survival
A large fraction of the planet’s energy resources is a result
of photosynthetic activity, from recent or past times.
Photosynthesis is the process used by plants to convert solar
energy into chemical compounds, which is responsible for
the maintenance of life of heterotroph beings and involves
photochemical processes (activated by the presence of light),
enzymatic processes that require no light, and diffusion
processes that are responsible for carbon dioxide and oxygen
exchanges between chloroplasts and atmospheric air
(STIRBET et al., 2020).
Photochemical processes occur in thylakoids inside
chloroplasts, where oxidation process of water molecules
occur, as well as reductions of NADP+ to NADPH, and
synthesis of ATP, which are essential compounds for the
enzymatic step which occurs in the stroma of chloroplasts.
NADPH and ATP are used to reduce atmospheric CO2,
incorporate CO2 in organic molecules, the carbohydrates,
which are the main sources of energy for growth and
development of plants. The incorporation of C occurs
through a cyclical sequence of reactions, termed pentose
cycle or Calvin-Benson cycle (GEIGER; SERVAITES, 1994;
TAIZ; ZEIGER, 2017).
Fixed C can be allocated from source tissues for storage
(as starch in chloroplast or saccharose in the cytosol), or
transported when the fixed C is incorporated into transport
sugars that are taken to the different drain tissues; in addition,
part of it can be temporarily stored in the vacuole and used
for metabolic processes in source and drain tissues to meet
energy demands and provide C skeletons for synthesis of
other compounds needed by the cell (LAVIOLA et al., 2007;
TAIZ et al., 2017).
Plants have leaf structures to capture CO2, the stomata,
which conduct gas exchanges with the atmosphere. Under
ideal climate conditions of light, temperature, and water
availability, stomata capture CO2 and release water vapor to
the atmosphere. Under prolonged drought conditions,
decreases in Ψw in leaves result in decreases in
photosynthesis, affected by decreases in stomatal
conductance (Table 2). Therefore, the CO2 availability for
fixation process is limited and the carbohydrate production
is reduced.
Table 2. Percentage of reduction in stomatal conductance (gs) and CO2 assimilation rate (A) in plant species under drought conditions.
Tabela 2. Porcentagem de redução da condutância estomática (gs) e taxa de assimilação de CO2 (A) em espécies sob condições de seca.
2.3. Drought as factor of regulation of C allocation in
plants
2.3.1. Allocation, translocation, and partition of
photosynthates
It is important to define the terms allocation,
translocation, and photosynthate partition, as studies present
different definitions for these terms, causing, in some cases,
confusion between definitions or omissions.
Allocation refers to regulation of the distribution of the
assimilated C in the source organ (leaf) for storage,
metabolism, and transport as starch or sugars (HASIBEDER
et al., 2015; TAIZ et al., 2017). The fixed C can be
incorporated into transport sugars that are taken from the
production areas to importing organs (drains), including
short- and long-distance transports. This transport is termed
translocation. Partition refers to the differential distribution
of photosynthates among the different drains, which is a
process that depends on the drain force of the assimilated C
according to its size and activity (TAIZ et al., 2017).
Similar to photosynthesis, these processes are affected by
water deficit, since they are connected to photosynthetic
metabolism products. However, the present review is
focused on a more investigative form of C allocation, which
can vary over the plant life cycle, according to the age of
different organs, and is affected by environmental conditions,
such as droughts, high temperatures, and low rainfall and
relative air humidity (OLIVEIRA et al., 2019).
All organic compounds inside the plant that can be
reintroduced or recycled in the primary metabolism can serve
as C reserves when C requirement exceeds the C supply by
the photosynthesis. Most of these compounds are used for
other functions and storage. For example, sugars of low
molecular weight can be used as intermediate metabolites, C
transport compounds, osmolytes, and C sources for
structural growth or respiration. The multifunctional nature
of many compounds denotes that they cannot be completely
degraded in live tissues, even when the plant is passing
through strong stressful conditions (HOCH, 2015).
Species
Stomatal
conductance (g
s
)
CO
2
assimilation
rate (A) References
Decrease (%)
Faia europeia (
Fagus sylvatica
L.)
48
37
(RUEHR
et
al.,
2009)
Sugarcane (
Saccharum offinarum
)
59.99
63.93
(GONÇALVES
et
al.,
2010)
Conilon Coffee (
Coffea canephora
)
92.8
65
(SILVA
et
al.,
2010)
Alamo tremedor (
Populus tremuloides
Michx.)
86.6
82
(GALVEZ
et
al.
,
2011)
Calendula (
Calendula officinalis
L.)
95.25
91.87
(PACHECO
et
al.,
2011)
Mutambo (
Guazuma ulmifolia
Lam.)
57.27
72.55
(SCALON et al., 2011)
Mogno africano (
Khaya ivorensis
)
95
90
(ALBUQUERQUE et al., 2013)
Pata
-
de
-
elefante (
Beaucarnea recurvata
)
80
92
(BERTOLLI et al., 2015)
Maize
(Zea mays)
12.8
26.57
(ANJUM et al., 2016)
Cowpea (
Vigna unguiculata
)
62.33
52.66
(SOUZA et al., 2020)
Effects of droughts on carbon allocation in plants
Nativa, Sinop, v. 10, n. 2, p. 142-153, 2022.
146
Despite the large number of compounds that can be used
as reserve, only two classes are synthetized exclusively as
storage compounds, which are polysaccharides (starch and
fructan) and neutral lipids (triacyclglycerols), the latter is
important, quantitatively, in only a small number of species
(HOCH, 2015). Studies that show C reserves term
compounds such as starch plus sugars of low molecular
weight as non-structural carbohydrates (NSC)
(WOODRUFF; MEINZER, 2011; HOCH, 2015).
Growth and other physiological functions of plants
depend on momentaneous photosynthetic rates and NSC
reserves. When the photosynthesis produces more C than
that required by the plant, part of the C is stored as NSC,
whose concentrations determine the balance between fixed
C and demanded C for growth, respiration, defense
metabolism, reproduction, and exudates (WOODRUFF;
MEINZER, 2011).
NSC accumulation is affected by water availability; a low
water availability affects cell expansion rates driven by the
turgor. Decreases in turgor of tissues decrease the
translocation from source to drain, and the assimilated C is
incorporated as sugars or converted into starch for storage,
resulting in accumulation of C allocated as NSC, providing
energy for metabolic processes for plant survival.
Under water stress conditions, plant growth rates are
lowered before the photosynthesis and respiration, resulting
in a more intense decrease in aerial growth than that in the
root system growth (Figure 2). More significant decreases in
aerial growth result in intense accumulation of NSC, with
high amounts of sugars. Roots depend exclusively on fixed C
in leaves, which is exported in high amounts for maintenance
of roots, despite the export speed be reduced.
Maintenance of root system to the detriment of shoot
growth was reported for Arabidopsis thaliana. The water deficit
decreased the shoot growth, but increased NSC
accumulation and resulted in a higher C allocation in roots.
The root system growth was little affected, with different
intensities of decrease between the growths of lateral roots
and main root, thus presenting little interference (DURAND
et al., 2016). The decreases in growth found for lateral and
main roots indicate that the plant may have undergone an
acclimatization process, prioritizing the growth of the main
root, since it can reach greater depths, thus increasing water
absorption, as deeper regions are less prone to water loss than
soil surface layers where lateral root grow.
NSC accumulation in drought conditions was previously
identified by Woodruff; Meinzer (2011), who analyzed the
seasonal course of NSC in Pseudotsuga menziesii with heights
of 2 to 57 m. Higher NSC accumulations were found in
leaves, followed by branches and shoots; starch was the main
component, followed by saccharose. The greater NSC
accumulation in the leaf is because it is the organ responsible
for C assimilation and synthesis of sugar and has larger
number of live cells that can convert and store NSC, resulting
in decrease of photosynthetic rates and in maintenance of cell
turgor.
The positive correlation between plant height and NCS
accumulation and the negative correlation between plant
heights and water and osmotic potentials are also important,
as proved for A. thaliana: regardless of the higher C
accumulation, the C allocated for aerial growth was low. The
highest heights found for P. menziesii plants were because tall
trees are subject to greater gravitational effects and greater
hydraulic resistance as the soil moisture decreases, therefore,
the stress increases and taller trees present higher stress levels
(WOODRUFF; MEINZER, 2011).
Therefore, a low Ψw reduces the plant growth, resulting
in lower biomass accumulation, which is connected to the
plant production. Thus, plant growth and biomass
production present the same dynamics, favoring root growth,
as found for A. thaliana, which, although presented decreases in
dry weight for both organs, it was less significant for roots when
compared to the control (DURAND et al., 2016), again denoting
the greater impact of water deficit on the plant aerial part, which
results in lower grain yield (SANTOS et al., 2012; ARRUDA et
al., 2015).
In addition to stress caused by drought, the factors
species and ontogeny also affect C allocation, and different
strategies of allocation can be found for a same genotype, as
they show variations in sensitivity to stress.
The growth of a same plant species in different regions is
possible due to the plant phenotypic capacity for
acclimatization, which can result in different levels of
sensitivity to stress in different environments. Regier et al.
(2009) induced to drought conditions two clones of Populus
nigra (Alamo negro) from contrasting climatic origins, one of
them adapted to drought (Poli) and other sensitive to drought
(58-861). The responses presented for accumulations of total
NSC (starch, saccharose, glucose, and fructose) and soluble
sugars (saccharose, glucose, and fructose) were different
between the clones. Sensitive plants presented decreases in
total NSC contents in leaves and roots, and the opposite was
found for adapted plants. Soluble sugar contents decreased
only in leaves of sensitive plants with accumulation in roots,
whereas adapted plants had decreases in leaves and roots.
Roots are the main reserve organ in the plant, and
decreases in starch contents in roots observed in plants
sensitive to stress can be connected to a high activity of the
enzymes that perform the hydrolysis of this compound to
provide substrate for the respiration process for growth or
maintenance. Whereas the accumulation of starch in roots of
plants adapted to drought conditions indicates that even
under stress conditions they prioritize growth and storage
and can allocate higher amounts of compounds for roots,
favoring their development and increasing their capacity to
absorb water and minerals.
The same result found for plants adapted to drought
conditions was found for seedlings of Populus tremuloides
(Alamo tremedor) subjected to drought under protected
environment conditions. In general, total NSC
concentrations in roots were 73.7% higher than those found
in seedling roots used as control (GALVEZ et al., 2011).
Similar results were found for plants of the same species
under mountain pasture conditions and subjected to drought
in the field.
The examples presented referring to different species and
studies showed that each species, under water deficit
conditions, presents specific dynamics that are sometimes
similar; however, their dynamics cannot be compared
because of the different experimental conditions and growth
stages. Moreover, the definition of drought effects cannot be
treated in a general approach, but with a distinction between
the investigations adopted to clearly assess the reaction of
each species separately.
2.3.2. Root exudates
Plants release exudates through the root system, which
are complex and soluble mixtures of C compounds, such as
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Nativa, Sinop, v. 10, n. 2, p. 142-153, 2022.
147
sugars, amino acids, organic acids, and secondary
metabolites, reaching up to 10% of the plant photosynthates,
composing a dynamic source of C to the soil and promoting
maintenance of ecosystems (FELLBAUM et al., 2012; LU et
al., 2018).
An intriguing question about exudates is: why plants
release significant quantities of a resource that is essential for
them? The answer is given by the interaction between plants
and soil microorganisms, known as symbiosis (FELLBAUM
et al., 2012).
Symbiosis has a cost-benefit relation in which plants
regulate the C allocation for microorganisms in response to
changes in environmental conditions, making C availability
to promote microbial growth in the soil, and microorganisms
provide significant quantities of nutrients to plants, such as
nitrogen, affecting plant phenology, triggering flowering,
stimulating growth, and increasing reproduction. Therefore,
exudates are important for the communication between plant
and microorganisms (FELLBAUM et al., 2012; LU et al.,
2018).
Droughts have a potential to change the soil
microorganism community and C availability through the
production of exudates by plants. The response of a
community to a stressful environment depends on the
physiological tolerance and metabolic flexibility of the
microorganisms; therefore, droughts affect the selection of
resistant or tolerant microorganisms, and the C availability
promotes organic matter decomposition through them and,
consequently, availability of nutrients for both symbiotic
microorganisms and plants.
The use of 13C isotope tracer is an important
methodology for studies evaluating C allocation, exudates,
respiration, and community of microorganisms in
underground systems. For example, decreases in respiration
and allocation of momentarily assimilated 13C to the soil
microbial mass was found for plants of Fagus sylvatica
(RUEHR et al., 2009). Decreases in the respiration process
was also found by Hasibeder et al. (2015) in mountain
pastures, resulting in lower soil C availability.
Mountain pastures were also evaluated by Fuchslueger et
al. (2013), who assessed changes in the microbial
communities and amount of available 13C to them and found
significant increases in fungal and bacterial biomasses in
treatments under drought conditions, with lower recently-
assimilated 13C availability in bacteria, but not for fungi, when
the transfer of 13C was not affected by drought.
The association of fungi with plant roots can increase
nutrient and water availability to the root system, as a higher
soil volume is explored, reaching depths inaccessible by roots
(FUCHSLUEGER et al., 2014; CHITARRA et al., 2016).
Therefore, this lack of changes in 13C allocated to soil fungi
may compose a strategy of plants to survive under water
deficit conditions. Another possible survival strategy in
pastures was the great capacity of plants to stimulate the
microbial activity and mineralization of nutrients, even when
the quantities of exudates were significantly reduced by the
drought (VRIES et al., 2019).
Droughts not only reduce the amount of exudates and C
allocated in them, but their quality. For example, Gargallo-
Garriga et al. (2018) evaluated plants of Quercus ilex and found
release of exudates consisted mainly of secondary
compounds (flavonoids, terpenoids, and phenols),
corresponding to approximately 71% of the total
metabolites, whereas 81% of exudates corresponded to
primary metabolites (saccharides, amino acids, and organic
acids) under recovery conditions (after a drought period).
Secondary organic compounds are highly specific and
important for the species evolution and interaction between
organisms, which are connected to plant defense
mechanisms against biotic and abiotic stresses, as primary
compounds are connected to plant growth and development.
This explains the dominance of secondary compounds in
exudates of Quercus ilex found by Gargallo-Garriga et al.
(2018) under drought conditions; the plants activated their
defense metabolism against the abiotic stress and produced
more primary compounds in rehydration condition as a
strategy for fast recovery of their functions and growth.
2.3.4. Phloem and metabolism of defense
The connection and transport of C from the shoot to the
root system occurs through the phloem tissue, which is in the
center of structural functions of the plant, transporting C as
NSC, nutrients, defense compounds, and all types of
information throughout the plant body. The capacity of the
phloem to transport compounds is controlled by the balance
of C and water flows inside the plant. Therefore, it is
expected that droughts affect the phloem function, as the
amount of available water and the photosynthate production
are reduced (SALMON et al., 2019).
Water is the main substance for dilution of organic and
mineral solutes. Water enters the root system and is
redistributed to all plant tissues through the xylem, which is
also responsible for supplying the phloem. When the soil
presents low Ψw, the amount of water transported through
the xylem and made available to the phloem is reduced,
leaving a more viscose solution. In addition to the phloem
texture, droughts can modify the anatomy of conducting
elements, decreasing their radius and the speed of recently
assimilated C (SALMON et al., 2019; DANNOURA et al.,
2019).
The increase in viscosity and decrease in radii of phloem
elements were reported by Dannoura et al. (2019), who
investigated effects of droughts on phloem anatomy and
transport in Fagus sylvatica and found that plants treated with
droughts had an increase of 0.41 mPa in viscosity as response
to a high carbohydrate accumulation in the phloem, and a
decrease of 3 μm in the radius of phloem elements, with a
decrease of 70% in the phloem hydraulic conductivity.
The effects of the decrease in radii of conducting elements
result in lower C allocation rates to the different organs and
metabolic pathways, thus increasing the time of permanence of
temporarily assimilated C in the leaf biomass of F. sylvatica L. and
mountain pastures (RUEHR et al., 2009; FUCHSLUEGER
et al., 2014).
Investigation in mountain pastures was more detailed by
Hasibeder et al. (2015), who made distinction between the
13C allocated and the speed of allocation in compounds such
as starch, saccharose, glucose, and fructose in shoots and
roots. They found no effect of the drought treatment on the
shoot, but found a decrease in the amount of C allocated, and
delay in the speed of allocation to roots, which was five days
for starch, 20 hours for saccharose, and 10 days for glucose
and fructose. The authors also investigated the speed of 13C
allocated to the respiration and found significant decreases in
the treatments, with concentrations of breathed 13C reaching
peaks of 8 and 24 hours after marking for control plants and
24 hours for plants under stress.
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Nativa, Sinop, v. 10, n. 2, p. 142-153, 2022.
148
Hasibeder et al. (2015) also found a significant increase in
saccharose, glucose, and fructose concentrations in the root
system, approximately 41% for saccharose over two weeks
after marking with 13C, and glucose and fructose
concentrations more than doubled during one and two weeks
of treatment.
The results indicate that drought conditions modulate the
allocation of recent assimilates to favor reservoirs of
carbohydrates as soluble organic compounds, mainly
saccharose. These syntheses of soluble organic compounds
are due to a defense strategy defense of osmotic adjustment,
which allows the plant to keep the integrity of its cells and
membranes by maintaining cell turgor; however, this
accumulation of osmolytes is the main process that competes
with the loading of phloem, decreasing the amount of C for
exports.
The osmotic adjustment is a physiological/molecular
response to water deficit by two ways: production of soluble
organic compounds and absorption of ions from the soil or
other organs. However, the use of ions in the osmotic
potential regulation can cause harmful effects to cell
metabolism when at high concentrations (SILVENTE et al.,
2012).
However, the production of osmolytes, or compatible
solutes, does not destabilize the membrane or affect
enzymatic functions, acting as protectors for them
(KRASENSKY; JONAK, 2012; SILVENTE et al., 2012).
The most common compatible solutes are amino acids,
such as proline, mannitol (sugar alcohols), and betaine glycine
(ammonium quaternary compound) (ALBUQUERQUE et
al., 2013; MONTEIRO et al., 2014). The synthesis of these
solutes is an active metabolic process that requires a large
amount of energy, and the amount of C used in this process
can be high.
Considering these compounds, proline is very important
for plants under water stress, and presented increases in
several studies (Table 3), in which the highest increases were
found for plants of Lippia sidoides Cham. and Khaya ivorensis:
approximately 13 and 16.5-fold, respectively.
Table 3. Studies that found increases in proline levels in plants under
drought conditions.
Tabela 3. Estudos que identificaram aumento nos teores de prolina
em plantas sob condições de seca.
Species Increase Authors
μmol g
MF
-
1
Coffee 4.12 (SILVA et al., 2010)
Peanuts 0.47 (PEREIRA et al., 2012)
Tomato 15.59-28.3 (CHITARRA et al., 2016)
Lemon 65.04
(ZAHER-ARA et al., 2016)
Orange 51.69
Alemow 60.51
Bael 66.71
Lemon 13.54
Red Blush 16.24
Orange 2.33
Pineapple 83
Shel 3.86
μmol g
MS
-
1
Rosemary 0.94 (ALVARENGA et al., 2011)
Papaya 13.93 (SILVA et al., 2012)
Mogno 42.28 (ALBUQUERQUE et al., 2013)
The proline accumulated during water stress conditions
does not act only as an osmolyte, but as a signaling and
defense molecule against oxidative damages. In the
cytoplasm, it promotes stabilization of protein structure,
assists in the maintenance of pH and redox status, decreasing
the amount of oxygen radicals responsible for thylakoid
membrane lipid peroxidation (KHAN et al., 2018).
The synthesis and accumulation of this amino acid are
found usually higher in leaves because of a need for
regulation of cell osmotic pressure to increase their water
retention capacity, thus limiting losses by transpiration. The
proline content in leaves can continue to increase even after
the beginning of irrigation, which can contribute to a fast
recovery of the plant water status (SILVA et al., 2012;
ALBUQUERQUE et al., 2013).
The proline content varies according to the plant
sensitivity level to water stress; however, it increases in all
cases under deficit water conditions (Table 4), as resistant
plants express greater capacity to synthesize this compound,
increasing its concentration.
As proline, other compounds are responsible for osmotic
adjustment, decreasing cell dehydration and protecting
membranes. These compounds include saccharose and
glycine betaine, which also present expressive accumulation
in leaves when compared to that in the root system (SILVA
et al., 2012; ZAHER-ARA et al., 2016)
These higher concentrations in leaves are connected to
the transpiration process, which is more intense in these
organs, and the increase of resistance to water loss promoted
by the osmotic adjustment makes the plant more resistant to
drought conditions. However, osmotic adjustment does not
occur only in leaves, the root system also has such capacity,
as this plant structure is in direct contact with the low Ψw of
soil and cannot easily regulate water loss.
The water stress caused by drought is usually combined
with other environmental factors, such as high temperatures,
which are intensifiers of the drought effect by increasing
evapotranspiration, affecting fluidity of lipids in cell
membranes, which can compromise their integrity and
inactivate enzymes in chloroplasts and mitochondria.
However, stressful processes can activate and increase
the activity of antioxidant enzymes, decreasing the amount of
reactive oxygen species (ROS) originated from the
incorporation of electrons to molecular oxygen that would be
used to reduce NADP+ into NADPH in chloroplasts
(CARVALHO; CARVALHO NETO, 2016).
ROS are highly oxidizing substances, and the most
known and studied are the triplet state of chlorophyll (3Chl*),
single oxygen (1O2), superoxide (O2–), hydroxyl (OH–), and
hydrogen peroxide (H2O2), which can damage cell structures
through the removal of electrons from several molecules,
including proteins, lipids, DNA, and carbohydrates
(CARVALHO; CARVALHO NETO, 2016).
Plants have two defense lines against ROS. The first
involves the xanthophyll cycle, which acts in the following
steps: chlorophyll absorbs energy from photons and reaches
an excited state, this excitation energy can be rapidly
photochemically dissipated (photochemical quenching); if
this dissipation is not rapid, a super photosystem excitation
occurs and the excited chlorophyll can react with molecular
oxygen forming reactive oxygen species. The xanthophyll
cycle prevents the super photosystem excitation, releasing
excess energy as heat (non-photochemical quenching), thus
preventing ROS formation (TAIZ et al., 2017).
Gomes & Silva
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149
The second defense line consists of production of
enzymatic components (superoxide dismutase, catalase,
peroxidases, and glutathione reductase) to neutralize
oxidative damages and protect cell membranes
(BITTENCOURT; SILVA; 2018).
Considering these enzymes, superoxide dismutase is the
only responsible for the reaction against high O2– toxicity,
and peroxidases and catalase are responsible for removing
H2O2 radicals. Several studies have shown that the activity of
these enzymes increases under drought conditions. Increase
of the three enzymes were found in wheat and peanut plants
(CHAKRABORTY; PRADHAN, 2012; PEREIRA et al.,
2012), increase of catalase was found in sorghum
(MAGALHÃES et al., 2016), and increase of superoxide
dismutase and catalase was found in Populus nigra (REGIER
et al., 2009).
In these studies, increases in antioxidant enzyme activity
were connected to resistance to drought and can be used to
identify the plant sensitivity to water stress, as species tolerant
to stress express increasing antioxidant activity even under
severe stress conditions, and sensitive species also express
increase in enzymatic activity, but it decreases as the drought
becomes more severe as a response to high ROS
concentrations (CHAKRABORTY; PRADHAN, 2012).
Table 4. Average proline values in different plant genotypes subjected to water stress by suspension of irrigation.
Tabela 4. Valores médios de prolina em diferentes genótipos submetidos à estresse hídrico por suspensão de rega.
Crop Genotypes Control Stress Authors
μmol g MS-1
Wheat Anahuac 24.64 94.54 (FUMIS; PEDRAS, 2002)
IAC-24 19.09 80.63
Peanut
55 437 0.65 1.33
(PEREIRA et al., 2012)
BR 1 0.88 1.31
LBM Branco 1.00 1.29
LBR Branco 1.20 1.74
LViPE-06 1.23 1.67
Sugarcane RB867616 0.16 0.86 (MEDEIROS et al., 2013)
RB962962 0.21 0.76
Potato Euro bravo 1 130 (BÜNDIG et al., 2016)
Maxi 1 140
Most responses of plants to drought occurs as a function
of hormonal signaling, through a positive regulation of
abscisic acid (ABA), which is the stress hormone (TARDIEU
et al., 2018) and acts as main sign involved in the processes
of adaptation to droughts, including stomatal closure, which
is the first response of plants to water loss caused by water
stress (GONÇALVES et al., 2010; ALBUQUERQUE et al.,
2013; BERTOLLI et al., 2015).
Roots use the stored C to promote metabolism of ABA
under drought conditions, which is exported to leaves, where
the transpiration is more intense, causing stomatal closure
and decreasing photosynthesis in a short time. The function
of this hormone is to control the ionic balance in guard cells
through the regulation of influx and efflux of K+, Cl-, and
organic acids (CARVALHO; CARVALHO NETO, 2016).
The synthesis of ABA in roots can stimulate their growth
and, when translocated to the shoot, it can cause stomatal
closure and decreased leaf growth with subsequent abscission
(TARDIEU et al., 2018).
Leaf abscission and decreases in leaf area caused by ABA
are visible responses to water stress, through which the plant
reduces C and energy consumptions, allowing a higher
amount of assimilates to be directed to the root system,
prioritizing their growth to favor water absorption by
increasing the soil volume explored, also composing a
strategy to maintain the growth after the stress.
A. thaliana plants showed approximately four-fold
decreases in leaf area, culminating with a 30% decrease in
number of leaves and 80% in biomass accumulation
(DURAND et al., 2016). This result shows the pros and cons
of decreasing in leaf area; it allows an economy of the energy
demanded for the expansion process, but results in lower
photosynthetic area and consequent lower C assimilation and
carbohydrate formation, making NSC the main source of
energy.
Leaf abscission and decreases in leaf area are
acclimatization strategies of plants to environmental
variations; another important leaf tissue specialization is the
decrease in stomatal density, increase in opening of ostioles
(REGIER et al., 2009; SCALON et al., 2011), thickening of
leaves (REGIER et al., 2009), and decrease in stomata
opening time (GALVEZ et al., 2011; SCALON et al., 2011).
3. DISCUSSION
The plant environment may present several stressful
agents. Plants are subjected to several environmental factors
over time, such as high and low temperatures, high and low
solar irradiance, high salinity, nutritional deficiency, toxicity
by elements, droughts, and floods (ALVARENGA et al.,
2011; ARRUDA et al., 2015); they are sessile organisms, thus
they must thrive under these challenges that are imposed by
the environment (SOUZA; LÜTTGE, 2015).
Water is the main essential factor for survival of biological
life as we know it, without it no life exists. The importance
of water to plants can be evaluated by assessing the
constitution of plant tissues, which consist, on average, of
85% to 90% water (WOOD, 2005).
From the agriculture point of view, water is the most
limiting factor for agricultural production in the world.
Despite some plants are in regions with high water
availability, a holistic view should be presented, considering
that the world water availability level is a great problem, and
depending on the evolution of climate changes, it can be
aggravated due to the occurrence of more frequent and
intense droughts during plant development stages, which can
cause plant death (SCALON et al., 2011).
Effects of droughts on carbon allocation in plants
Nativa, Sinop, v. 10, n. 2, p. 142-153, 2022.
150
The occurrence of droughts alone is a great problem for
the maintenance of native and agricultural vegetations and
can be aggravated, considering the vegetation variability in
the environments. Drought situations diverge between
species (Table 1) and are dependent on their tolerance to
stress.
Severe water stress caused by drought conditions is
responsible for significant physiological and metabolic
changes in plants. Several responses to water scarcity have
been observed, and decreased growth is by far the most
significant (HASIBEDER et al., 2014; MONTEIRO et al.,
2014; ARRUDA et al., 2015).
The main growth promoting agent is water, which,
through the turgor pressure, promotes irreversible expansion
of cell wall. Thus, droughts affect the plant growth, mainly
by limiting water availability for cell expansion and decreasing
the amount of energy available for this process by decreasing
photosynthesis and carbohydrate production (PACHECO et
al., 2011; MEDEIROS et al., 2013).
Decreases in photosynthetic process occur because of
different reasons and are intensified by water scarcity due to
stomatal limitations for influx of CO2; damages to the
photosynthetic apparatus, mainly to the photochemical step;
reductions in energy production (ATP); and decreases in the
Rubisco enzyme activity or regeneration (MARENCO et al.,
2014). This enzyme is responsible for catalyzing C fixation
reaction.
A reduced Rubisco activity and regeneration decreases
the production of glyceraldehyde-3-phosphate (PGAL)
molecules used for synthesis of starch, sugars, and many cell
components. That means decreases in compounds used as
source of energy for the metabolic processes, inducing the
different uses of carbohydrates and their different allocations
(organs) (FUCHSLUEGER et al., 2014; BERTOLLI et al.,
2015; SOUZA; LU, 2015).
Percentages of decrease in the photosynthetic process
resulting from limitations in stomatal conductance are
presented in Table 2. The comparison between species shows
those with greater capacity to thrive in hostile environments
regarding water availability. Therefore, the plants that are
more able to survive in such conditions, present lower
percentages of decrease in stomatal activity and
photosynthesis. Considering the species presented here
which were evaluated under drought conditions, maize
presented the greatest capacity to maintain its metabolism
with no significant changes; this is because maize plants
present a C4 metabolism, which enables them to explore drier
environments using water more efficiently, in addition to
being an isohydric species which controls water loss through
chemical and hydraulic signs (TARDIEU et al., 2018).
Water shortage conditions result in low amounts of C
allocated to respiration (RUEHR et al., 2009; HASIBEDER
et al., 2015); increases in C allocation for defense metabolism,
with higher synthesis of ABA, osmoprotectant compounds
and antioxidants (ALBUQUERQUE et al., 2013;
MAGALHÃES et al., 2016); reduction in the radius of
phloem conducting elements; increase in phloem viscosity;
increase in C concentration in phloem; reduction of C
loading, discharge, and translocation and in the speed of
these processes (DANNOURA et al., 2019; SALMON,
2019); and decrease of leaf area, density and size of stomata,
number of structures, and crop yield (REGIER et al., 2009;
ARRUDA et al., 2015; DURAND et al., 2016).
The high production of osmoprotectant compounds,
such as proline which is widely studied in drought conditions,
can be used to identify tolerant species to water stress. Tables
3 and 4 show species/genotypes that grow low and high
amounts of this amino acid; those with higher production are
more tolerant to water scarcity. The fast increase in proline
content can also be a signaling denoting that the plant is
under a water stress condition (KHAN et al., 2018).
Therefore, the response of plants to lack of water
depends on the species; Bowdichia virgilioides, for example,
tolerate a higher stress level than the other species presented
in Table 1, which are more sensitive to water stress, according
to the definition of drought for them.
The species factor, which is specific for the definition of
climatic stress conditions, and the soil characteristics
determine the characteristics of the vegetation of each region.
For example, regions that have greater water availability, such
as the Amazon, tend to present taller plants, and regions with
lower water availability, such as the Cerrado and Caatinga
biomes, tend to present smaller plants, i.e., water availability
determines the genetic codes and metabolisms of plants that
developed in the environment (KRASENSKY; JONAK,
2012; SOUZA; LÜTTGE, 2015).
Plant species can be categorized according to their
dynamics under water scarcity into species that delay, escape,
or tolerate dehydration (BEWLEY, 1979). These categories
are determined according to plant acclimatization or
adaptation capacity, which includes different responses to
stress conditions.
Water stress affects the plant C balance, directly effecting
the crop yield; thus, it is an interesting factor for farmers. Low
crops yields can decrease food reserves, increase prices of
agricultural products, and decrease irrigation levels,
impacting the production chain of the agribusiness (FAO,
2004).
According to the United Nations Convention to Combat
Desertification (UNCCD, 2016), a proactive approach to
increase the resistance to drought is composed by three
bases: monitoring of droughts and use of early warning
systems that integrate different variables, such as rainfall
depths, stream flows, snow, underground water levels,
reservoir and lakes levels, and soil moisture; vulnerability and
risk evaluation, which adopt important resources, such as
record of impacts of droughts on economic sectors,
vulnerability reasons, and conditions that impact the
resistance of a system to drought, resilience of affected
communities, and assessment of sector, populational groups,
and ecosystems under high risk; and measures to mitigate the
risks of drought, which include capture of water, protection
of water sources, construction of dams, restoration of
pastures areas, planting of trees, improvement and
adequation of irrigation systems, and growth of crops
tolerant to drought.
Considering the three bases described by the UNCCD,
measures for mitigation can be the most used in rural
properties; the use of genetic resources is the main measure
used to reduce impacts of droughts on the production. An
example is the growing of species with different tolerance
levels to water stress, maintaining the production during
gradual or moderate soil water deficit. However, the choice
of species may consider the plant tolerance level to stress and
its dynamics when associated with the different
environmental factors and the interaction between them.
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151
Plants that present right tolerance level to stress usually
have morphophysiological characteristics that enable their
implementation, growth, and development, such as a leaf
orientation that avoids excessive warming and a consequent
transpiration; more developed and efficient root systems that
explore greater soil volume when searching for moisture;
presence of structures that reduce leaf water loss, such as
trichomes, thick cuticles, and lower leaf area; and protection
mechanisms, such as tolerance to desiccation, detox, and
recovery from emboli in the xylem (TARDIEU et al., 2018).
In addition to the use of tolerant species, farmers can use
no-tillage system; according to the Food and Agriculture
Organization (FAO, 2004) of the United Nations, it is
characterized by the maintenance of straw on the soil, which
is a practice used for conservation of soil moisture and
improvement of soil conditions.
4. CONCLUSIONS
The responses of plants to water stress conditions include
greater allocation of carbon for formation of non-structural
carbohydrates (energy source of metabolic processes for
plant survival); maintenance of root system growth for
production of volatile organic compounds (osmoregulation)
and antioxidant enzymes (defense metabolism); and
decreases of the carbon allocated for maintenance of aerial
growth and for root exudates, and decreases in speed of
carbon allocation caused by increases in viscosity of phloem.
However, these responses may present variations because the
origin and intensity of the effects are determined by the
species, ontogeny, and level of sensitivity of the plant to
stress.
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http://www.fao.org/3/y5744e/y5744e00.htm#Contents
Acesso em: 15 abr. 2021.
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